ArticlePDF AvailableLiterature Review

Abiotic Stress-Induced Leaf Senescence: Regulatory Mechanisms and Application

Authors:
  • Beijing Forestry University

Abstract

Leaf senescence is a natural phenomenon that occurs during the aging process of plants and is influenced by various internal and external factors. These factors encompass plant hormones, as well as environmental pressures such as inadequate nutrients, drought, darkness, high salinity, and extreme temperatures. Abiotic stresses accelerate leaf senescence, resulting in reduced photosynthetic efficiency, yield, and quality. Gaining a comprehensive understanding of the molecular mechanisms underlying leaf senescence in response to abiotic stresses is imperative to enhance the resilience and productivity of crops in unfavorable environments. In recent years, substantial advancements have been made in the study of leaf senescence, particularly regarding the identification of pivotal genes and transcription factors involved in this process. Nevertheless, challenges remain, including the necessity for further exploration of the intricate regulatory network governing leaf senescence and the development of effective strategies for manipulating genes in crops. This manuscript provides an overview of the molecular mechanisms that trigger leaf senescence under abiotic stresses, along with strategies to enhance stress tolerance and improve crop yield and quality by delaying leaf senescence. Furthermore, this review also highlighted the challenges associated with leaf senescence research and proposes potential solutions.
Citation: Tan, S.; Sha, Y.; Sun, L.;
Li, Z. Abiotic Stress-Induced Leaf
Senescence: Regulatory Mechanisms
and Application. Int. J. Mol. Sci. 2023,
24, 11996. https://doi.org/10.3390/
ijms241511996
Academic Editor: Martin Bartas
Received: 16 May 2023
Revised: 14 July 2023
Accepted: 19 July 2023
Published: 26 July 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
International Journal of
Molecular Sciences
Review
Abiotic Stress-Induced Leaf Senescence: Regulatory
Mechanisms and Application
Shuya Tan , Yueqi Sha , Liwei Sun * and Zhonghai Li *
State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology,
Beijing Forestry University, Beijing 100083, China
*Correspondence: lsun2013@bjfu.edu.cn (L.S.); lizhonghai@bjfu.edu.cn (Z.L.)
These authors contributed equally to this work.
Abstract:
Leaf senescence is a natural phenomenon that occurs during the aging process of plants and
is influenced by various internal and external factors. These factors encompass plant hormones, as
well as environmental pressures such as inadequate nutrients, drought, darkness, high salinity, and
extreme temperatures. Abiotic stresses accelerate leaf senescence, resulting in reduced photosynthetic
efficiency, yield, and quality. Gaining a comprehensive understanding of the molecular mechanisms
underlying leaf senescence in response to abiotic stresses is imperative to enhance the resilience and
productivity of crops in unfavorable environments. In recent years, substantial advancements have
been made in the study of leaf senescence, particularly regarding the identification of pivotal genes
and transcription factors involved in this process. Nevertheless, challenges remain, including the
necessity for further exploration of the intricate regulatory network governing leaf senescence and
the development of effective strategies for manipulating genes in crops. This manuscript provides an
overview of the molecular mechanisms that trigger leaf senescence under abiotic stresses, along with
strategies to enhance stress tolerance and improve crop yield and quality by delaying leaf senescence.
Furthermore, this review also highlighted the challenges associated with leaf senescence research
and proposes potential solutions.
Keywords: leaf senescence; abiotic stress; stress tolerance; transcription factor; Arabidopsis; crop
1. Introduction
The leaves of plants serve as the primary sites for photosynthesis, where light energy
is converted into chemical energy stored in carbohydrate molecules. These carbohydrates
serve as the main energy source for all living organisms on Earth. Senescence, the final
stage of leaf development, is a gradual and intricate biological process comprising initiation,
progression, and terminal phases [
1
,
2
]. In this process, the leaves gradually turn yellow,
shrivel, and fall off. During the later stages of leaf senescence, chlorophyll and chloroplasts
deteriorate, accompanied by the breakdown of macro-molecules like proteins, lipids, and
nucleic acids [
1
,
2
]. In annual plants, the nutrients released from senescent leaves are
transferred to actively growing young leaves and seeds to enhance reproductive success.
In the case of perennial plants, such as deciduous trees, nitrogen from leaf proteins is
redirected to form bark storage proteins in phloem tissues. These proteins are stored
throughout the winter and then mobilized and reused for spring shoot growth [
3
5
]. In
agriculture, senescence is capable of remobilizing leaf nitrogen and micronutrients into
the grain or fruit. The NAC transcription factor NAM-B1 plays an important role in the
regulation of expressions of nitrogen transport-related genes duringsenescence [
6
]. A recent
study revealed that OsDREB1C shortens lifespan but improves photosynthetic capacity
and nitrogen utilization, and transgenic plants with overexpression of OsDREB1C have
41.3% to 68.3% higher yields than wild-type plants [
7
]. Consequently, the timing of leaf
senescence plays a crucial role in facilitating nutrient cycling, environmental adaptation,
and reproduction in plants [8].
Int. J. Mol. Sci. 2023,24, 11996. https://doi.org/10.3390/ijms241511996 https://www.mdpi.com/journal/ijms
Int. J. Mol. Sci. 2023,24, 11996 2 of 17
The leaf senescence process is accompanied by changes in the expression of thousands
of senescence-associated genes (SAGs) [
9
]. Studies have shown that several transcriptional
regulators (TFs) regulate senescence by controlling SAG expression [
10
]. In one of them,
a number of NAC TFs were identified as core regulators of senescence [
11
13
]. EIN3,
a key TF that functions downstream of EIN2 in ethylene signaling pathway, increases
the transcript levels of ORE1/AtNAC092/AtNAC2 through the direct repression of miR164
transcription [
14
]. WRKY53 positively regulates leaf senescence [
15
] via targeting various
SAGs such as SENRK1 [16].
The initiation and progression of leaf senescence are influenced by various internal and
external factors [
1
,
2
,
8
]. Leaf senescence can be triggered as a defense mechanism in response
to biotic stress factors such as pathogen infection or insect damage. Additionally, abiotic
stress factors including drought, high salinity, high temperature, or nutrient deficiencies can
accelerate leaf senescence [
1
,
2
,
8
,
17
19
]. These stressors can induce oxidative stress, leading
to the accumulation of reactive oxygen species (ROS), which can cause DNA damage and
activate SAGs [1,2,8,17,18,20].
Numerous studies conducted on crops like wheat and rice demonstrated that mod-
ifying leaf senescence processes can have a significant impact on crop yield and qual-
ity. For instance, in apple trees (Malus domestica), improving fruit quality was achieved
by extending the lifespan of leaves through the modulation of senescence-associated
transcription factors, MbNAC25 and MdbHLH3 [
21
,
22
]. Similarly, in tomato (Solanum
lycopersicon), increasing fruit yield and sugar content was achieved by suppressing the
expressions of SIORESARA1 (ORE1) and SlNAP, which delayed leaf senescence [
23
,
24
].
Additionally, delaying leaf senescence in tobacco or cassava resulted in enhanced drought
resistance [
25
28
]. Therefore, gaining a deeper understanding of the regulatory mecha-
nisms underlying leaf senescence can aid researchers in developing more resilient plants
that can withstand environmental stresses. This, in turn, would lead to improvements
in crop yield, quality, and contribute to global food security and sustainability [
8
]. This
manuscript provides a comprehensive review of the molecular mechanisms involved in leaf
senescence induced by abiotic stresses such as nitrogen deficiency, drought, high salinity,
and extreme temperature. It also discusses strategies to enhance stress tolerance, crop yield,
and quality by delaying leaf senescence. Furthermore, the review highlights the challenges
associated with leaf senescence research and explores potential solutions.
2. Abiotic Stress-Induced Leaf Senescence
2.1. Nitrogen Deficiency-Induced Leaf Senescence
Nitrogen, an essential macronutrient in plants, plays a crucial role in leaf senescence,
and its deficiency triggers a rapid senescence process [
29
31
]. ORE1, a key regulator of
leaf senescence, was identified as a major factor in nitrogen deficiency-induced leaf senes-
cence [
29
,
30
]. In conditions of nitrogen deficiency, loss of ORE1 function results in delayed
senescence, while overexpression of ORE1 accelerates leaf senescence, characterized by
yellowing leaves, reduced chlorophyll content, and increased expression of SAG12 [
29
].
Interestingly, overexpression of nitrogen limitation adaptation (NLA) in ORE1 overexpress-
ing plants mitigates the leaf senescence phenotype induced by nitrogen deficiency. NLA,
which encodes a RING-type ubiquitin ligase [
32
], represses leaf senescence by promoting
the ubiquitination and degradation of the nitrate transporter NRT1.7 [
33
]. In a similar
mechanism, NLA interacts with ORE1 in the nucleus and regulates its stability through
polyubiquitination, with the involvement of PHOSPHATE2 (PHO2). PHO2 encodes an E2
ubiquitin-conjugating enzyme (UBC) and is responsible for maintaining cellular phosphate
homeostasis in Arabidopsis [
34
,
35
]. Consequently, nla and pho2 mutant plants exhibit
accelerated leaf senescence under nitrogen-starvation conditions, whereas nla/ore1 and
pho2/ore1 double mutant plants retain green leaves. These findings suggest that fine-
tuning the levels of ORE1 through post-translational modifications by NLA/PHO2 ensures
a regulated progression of senescence [
29
]. Interestingly, the deubiquitinases UBP12 and
UBP13 were identified as regulators of ORE1 stability by deubiquitinating polyubiquiti-
Int. J. Mol. Sci. 2023,24, 11996 3 of 17
nated ORE1 and increasing its stability [
30
]. Plants overexpressing UBP12 or UBP13 display
accelerated leaf senescence, which can be reversed by mutation of ORE1. Conversely,
overexpression of ORE1 exacerbates the senescence phenotype when UBP12 or UBP13
is also overexpressed [
30
]. These studies provided a model that explains the molecular
framework underlying the involvement of ORE1 in the regulation of nitrogen deficiency-
induced leaf senescence [
29
,
30
]. Under normal conditions, ORE1 is polyubiquitinated by
the E3/E2 enzyme complex, NLA/PHO2, and, subsequently, degraded by 26S proteasomes,
leading to delayed leaf senescence. However, under nitrogen-deficient conditions, UBP12
and UBP13 counteract the effects of NLA/PHO2 by deubiquitinating polyubiquitinated
ORE1, preventing its degradation. This elevated level of ORE1 activates the expression of
downstream SAG genes, thereby accelerating leaf senescence.
Recently, a zinc finger transcription factor called growth, development, and splicing 1
(GDS1) [
36
] was discovered to have a role in repressing leaf senescence induced by nitrogen
deficiency [
31
]. GDS1 functions as a crucial co-activator or co-protein in the early stages
of pre-mRNA splicing and is essential for growth and development in Arabidopsis [
36
].
Mutants of gds1 exhibit early leaf senescence, reduced NO
3
content, and impaired
nitrogen uptake under nitrogen-deficient conditions. Biochemical analysis revealed that
GDS1 can bind to the G-box motifs present in the promoter regions of phytochrome-
interacting factor 4 (PIF4) and PIF5, thereby repressing their expression [
31
]. PIF4 and
PIF5 were identified as regulators of dark- and heat-induced as well as age-triggered
leaf senescence in Arabidopsis [
37
40
]. Intriguingly, PIF4 and PIF5 also play a role in
nitrogen deficiency-induced leaf senescence. Under nitrogen-deficient conditions, delayed
leaf senescence was observed in pif4-2 and pif5-3 mutants compared to wild-type plants,
while transgenic lines exhibited accelerated leaf senescence phenotypes. Expression levels
of PIF4 and PIF5 in the leaves of wild-type plants were significantly higher under low
nitrogen conditions compared to high nitrogen conditions [
31
]. This research presents
a novel model to explain leaf senescence induced by low nitrogen levels [
31
]. Under
nitrogen-sufficient conditions, GDS1 binds to the promoters of PIF4 and PIF5, inhibiting
their expression and thereby suppressing the expression of downstream SAGs, resulting in
delayed leaf senescence. However, under nitrogen-deficient conditions, the accumulation of
anaphase-promoting complex or cyclosome proteins promotes the ubiquitination-mediated
degradation of GDS1, leading to the release of PIF4 and PIF5 repression. Consequently,
downstream SAGs are activated, promoting early leaf senescence.
Regarding both of these proposed models, which explain leaf senescence induced
by low nitrogen levels [
29
31
]: are they independent or do they have any relationship?
It was discovered that PIF4 and PIF5 directly bind to the promoter of ORE1, promoting
its expression, thereby accelerating leaf senescence. Conversely, GDS1 directly binds to
PIF4 and PIF5, repressing their gene expression and mitigating low nitrogen-induced leaf
senescence [
31
]. Future investigations will need to analyze whether GDS1 can directly
regulate ORE1 by binding to its promoters or indirectly influence its expression through
PIF4/PIF5. Additionally, it would be interesting to explore if PUB12/14 and NLA/PHO2
can interact with GDS1. Furthermore, the relationship between these two regulatory
pathways can be elucidated by generating multiple mutant combinations. These studies
will contribute to a deeper understanding of leaf senescence induced by low nitrogen levels.
2.2. Drought Stress-Induced Leaf Senescence
Drought stress is a significant abiotic stress factor that has detrimental effects on
plant growth and development [
41
], ultimately leading to leaf senescence [
42
]. The in-
volvement of a NAC transcription factor, NTL4, in drought-induced leaf senescence has
been identified [
43
]. Under normal conditions, there was no notable difference in the leaf
senescence process between wild type plants, transgenic plants overexpressing NTL4, and
ntl4 mutants. However, under drought conditions, leaf senescence was accelerated in the
transgenic plants while being significantly delayed in the ntl4 mutant. NTL4 promotes the
production of ROS by binding to the promoters of RBOHC and RBOHE under drought
Int. J. Mol. Sci. 2023,24, 11996 4 of 17
conditions. In turn, the elevated ROS production further stimulates NTL4 gene expression,
creating a feed-forward acceleration loop. Notably, NTL4 is expressed at basal levels dur-
ing vegetative growth stages and is rapidly induced in response to drought stress. The
induction of NTL4 expression under drought conditions is particularly evident in the distal
leaf area, where leaf senescence initiates upon exposure to drought stress [
2
]. In response
to drought, the distal regions of senescing leaves accumulate ROS and experience cell
death [
18
]. This response facilitates the transfer of nutrients and metabolites from senescing
leaves to absorptive organs and newly formed leaves, while minimizing water loss through
transpiration [
18
]. Thus, NTL4-mediated leaf senescence enhances the chances of plant
survival under drought conditions. Supporting this hypothesis, the overexpression of NAC
transcription factors ANAC019,ANAC055, and ANAC072 leads to early leaf senescence but
increases drought tolerance [
44
]. Additionally, it has been found that the ABA receptor
PYL9 promotes leaf senescence and enhances drought resistance [
45
]. By activating the
signaling cascade of PP2Cs-SnRK2s-RAV1/ABF2-ORE1, the ABA receptor PYL9 promotes
drought resistance by reducing transpirational water loss and triggering dormancy-like
responses such as senescence in old leaves and growth inhibition in young tissues under
severe drought conditions [
45
]. The accelerated leaf senescence observed in transgenic
plants overexpressing PYL9 (under the control of the pRD29A promoter) aids in generat-
ing a greater osmotic potential gradient, thereby allowing water to preferentially flow to
developing tissues [45].
Nonetheless, when exposed to severe drought conditions, the expression of NTL4 and
the accumulation of ROS extend throughout the entire plant, resulting in necrosis of the
entire plant body [
28
]. This observation suggests that delaying leaf senescence could poten-
tially enhance drought tolerance. Under drought stress, maintaining a balance between
growth and survival is crucial for the overall fitness of plants [
46
], yet the mechanisms
underlying this balance remain poorly understood [
8
]. Gaining a deeper understanding of
the molecular mechanisms involved in drought-induced leaf senescence holds promise for
developing strategies to alleviate the detrimental effects of drought stress on plant growth
and productivity [
18
]. In this regard, NTL4 emerges as a potential candidate gene for
coordinating plant stress tolerance and growth by precisely regulating its gene expression
to initiate leaf senescence at the appropriate time.
2.3. Salt Stress-Induced Leaf Senescence
Salinity, a significant environmental stressor, particularly in arid and semi-arid regions,
poses a substantial threat to crop productivity, leading to significant crop losses [
47
,
48
]. Salt
stress exerts its negative impact on crop growth through various mechanisms, including
osmotic stress, toxicity from specific ions, nutrient imbalances, and disrupted hormonal
regulation [
49
51
]. It is estimated that more than 6% of the Earth’s land is affected by
salinity, with approximately 20% of irrigated land being saline, resulting in substantial
agricultural losses amounting to tens of billions of dollars annually [
52
54
]. The effect of
salt stress on plant senescence varies depending on the salt concentration. Mild salt stress
can induce early flowering in plants, while severe salt stress can trigger leaf senescence and
cell death [17].
Several research studies focused on identifying transcription factors involved in the
regulation of salt stress-induced leaf senescence [
55
,
56
]. One prominent family in this
context is the NAC transcription factor family, which has been extensively studied for its
role in salt stress-induced leaf senescence [
55
]. ANAC092/ORE1, a member of this family,
was found to contribute to salt-promoted senescence by controlling gene expression in
response to salt stress [
57
]. Overexpressing ORE1 leads to salt-induced senescence, while
ANAC092 knockout plants exhibit delayed senescence [
57
]. Ethylene-insensitive 3 (EIN3), a
key transcription factor in the ethylene signaling pathway, acts as an upstream regulator
of ORE1, influencing both leaf senescence and the response to salt stress [
14
,
58
]. Conse-
quently, the age-dependent trigeminal feed-forward pathway involving ANAC092/ORE1
Int. J. Mol. Sci. 2023,24, 11996 5 of 17
potentially intersects with other developmental and environmental signals to govern leaf
senescence and cell death processes [56].
ANAC016 and ANAC032 are additional transcription factors that contribute to the
positive regulation of leaf senescence under salt stress by controlling the expression of
SAGs [
59
61
]. Mutants of nac016 were found to retain their green phenotype under salt
stress conditions, while plants overexpressing NAC016 exhibit rapid senescence [
59
]. Simi-
larly, the expression of ANAC032 was induced by salinity and promotes leaf senescence
in response to salt stress [
61
]. Notably, the ANAC032OX line showed increased accumula-
tion of hydrogen peroxide (H
2
O
2
), whereas the chimeric repressor line (ANAC032-SRDX)
exhibited reduced H
2
O
2
levels [
61
]. These findings suggest that the altered responses of
ANAC032 transgenic lines to salt stress may involve differential accumulation of ROS [
61
].
ANAC047, another transcription factor induced by salinity, is also implicated in salt stress-
induced senescence [
62
]. Transgenic plants expressing the chimeric inhibitor ANAC047-
SRDX displayed enhanced salt tolerance, indicating that ANAC047 acts as a positive
regulator of stress-induced senescence [
62
]. Conversely, ANAC083/VNI2 functions as a
negative regulator of senescence in Arabidopsis [
63
]. Plants with high expression levels
of ANAC083 exhibited significant salt and drought tolerance, along with delayed senes-
cence [
63
]. Moreover, increased ANAC083 expression led to the upregulation of COR/RD
genes [
63
]. ANAC042/JUNGBRUNNEN1 (JUB1), another negative regulator of senescence,
promotes plant longevity and confers tolerance to abiotic stresses such as heat and salt
in Arabidopsis [
64
]. JUB1 expression is rapidly induced by the accumulation of H
2
O
2
,
and its overexpression results in delayed natural senescence [
64
]. Recently, a transcription
factor from the AP2/ERF family, ethylene-responsive factor 34 (ERF34), was identified as
a negative regulator of salt stress-induced leaf senescence and a contributor to salt stress
tolerance [
56
]. ERF34 directly binds to the promoters of early responsive to dehydration
10 (ERD10) and responsive to desiccation 29A (RD29A), activating their expression [
56
].
This study suggests that ERF34 may serve as a potential mediator that integrates salt stress
signals with the leaf senescence program.
The pivotal role of stress response transcription factors as key regulators of leaf senes-
cence was extensively demonstrated in crops and trees [
65
67
]. For instance, overexpression
of the rice NAC gene SNAC1 in transgenic cotton enhances drought and salt tolerance by
promoting root development and reducing transpiration rate [
68
]. In rice, the salt stress re-
sponse gene ONAC106 acts as a negative regulator of leaf senescence [
69
]. Gain-of-function
mutants of ONAC106, such as ONAC106-1D transgenic plants with a 35S enhancer inserted
into the ONAC106 gene’s promoter region, exhibited delayed senescence and improved
salt stress tolerance [
69
]. Similarly, the overexpression of ShNAC1 in Solanum habrochaites
delays salt stress-induced leaf senescence [
70
]. In Populus euphratica, the overexpression of
two NAC transcription factors, PeNAC034 and PeNAC036, results in enhanced salt stress
sensitivity and tolerance, respectively [
71
]. Notably, PeNAC034 overexpression promotes
leaf senescence, while PeNAC036 overexpression inhibits it [
72
]. In addition to transcription
factors, other regulatory genes also play a crucial role in salt-induced leaf senescence.
In rice, the loss of function of the receptor-like kinase gene bilateral blade senescence 1
accelerates leaf senescence and reduces salt tolerance [73].
The overexpression of the salt-inducible protein salT in rice was shown to delay leaf
senescence, potentially serving as a feedback regulation to suppress salt stress-induced
senescence [
74
]. Furthermore, a comparative transcriptome analysis of Arabidopsis plants
exposed to age-dependent and salt stress-induced leaf senescence revealed potential molec-
ular mechanisms underlying the interplay between these two senescence scenarios, includ-
ing the involvement of H
2
O
2
-mediated signaling [
75
]. Salt stress-induced leaf senescence
is a complex process regulated by multiple genes and signaling pathways. However, the
intricate mechanisms that integrate salt stress signaling with the leaf senescence program
remain largely elusive [
56
]. Enhancing our understanding of the molecular mechanisms
underlying salt-induced leaf senescence will contribute to the development of strategies
aimed at improving plant stress tolerance and crop productivity [8].
Int. J. Mol. Sci. 2023,24, 11996 6 of 17
2.4. Darkness-Induced Leaf Senescence
Light plays a crucial role in plant growth, morphology, and development [
76
]. How-
ever, when plants are exposed to shade or complete darkness for an extended period,
it triggers leaf senescence [
37
,
77
81
]. Transcriptomic analysis has shown that gene ex-
pression changes induced by darkness closely resemble those observed during natural
senescence [
82
85
]. In fact, more than 50% of the genes up-regulated during natural
senescence are also up-regulated under dark treatment conditions [
83
]. As a result, dark
treatments are widely employed as a rapid, convenient, and effective method to induce leaf
senescence, making it easier to investigate the impact of additional regulators of senescence,
such as phytohormones, sugars, and secondary metabolites [8,83].
Recent investigations unveiled several genes and signaling pathways associated with
dark-induced leaf senescence. To identify mutants with delayed dark-induced senescence,
an experiment utilizing an individually darkened leaf (IDL) setup was conducted on Ara-
bidopsis thaliana Col-0 plants treated with ethyl methanesulfonate mutagenesis [
80
]. The
study revealed that PIF5 loss-of-function mutants, specifically pif5-621, exhibited signifi-
cantly delayed chlorophyll loss in the IDL [
80
]. Remarkably, the overall growth habit of
pif5-621 resembled that of wild-type plants, indicating a direct impact of the pif5 muta-
tion on senescence rather than an indirect effect through life cycle progression or overall
growth [
80
]. One plausible hypothesis to explain the extended lifespan of pif5-621 IDLs is
that the cells decelerated their metabolism, particularly respiration, to minimize carbon
consumption and prolong survival compared to wild-type IDLs. Supporting this notion, pif
quadruple mutants (pifQ)pif1 pif3 pif4 pif5, which exhibit a constitutive photomorphogenic
phenotype when grown in the dark, maintained green cotyledons even after 10 days of
dark treatment, while cotyledons of the wild type turned completely yellow, indicating that
PIFs promote senescence under light-deprived conditions [
38
,
40
]. PIF4 and PIF5 influence
ABA signaling by modulating ABSCISIC ACID INSENSITIVE 5 (ABI5) and ENHANCED
EM LEVELS (EEL), two sister genes encoding basic leucine zipper (bZIP) class A tran-
scription factors, which exhibited significantly reduced induction after darkening in pifQ
mutants compared to the wild type [
40
]. Correspondingly, the single mutants abi5,eel,
and, particularly, the abi5 eel double mutant displayed delayed senescence under dark
conditions. Furthermore, PIF4 or PIF5 stimulates ethylene signaling by directly regulat-
ing the transcription of EIN3 [
40
]. Additionally, ethylene evolution is diminished in pif4
mutants and elevated in PIF4 and PIF5 overexpressors [
38
,
86
]. Treatment of pif4 mutants
with ethylene partially restored the senescence phenotype, indicating that PIFs promote
dark-induced senescence by inducing ethylene biosynthesis and signaling. Moreover, PIF4,
PIF5, and their target transcription factors (ABI5, EEL, and EIN3) directly activate the
transcription of ORE1, suggesting the establishment of multiple coherent feed-forward
regulatory circuits involving these transcription factors to induce leaf senescence [
37
]. As
expected, ein3 and ore1 mutants exhibited a significant delay in senescence compared to
the wild type, as evidenced by higher chlorophyll content and Fv/Fm levels under dark
conditions [
14
]. PIF4/PIF5 directly activates the expression of ABI5 and EIN3, which, in
turn, activate the transcription of ORE1. ORE1 collaborates with PIFs, ABI5, and EIN3 to
up-regulate genes involved in chlorophyll degradation, including staygreen 1 (SGR) and
non-yellow coloring 1 (NYC1) [
38
,
40
,
87
]. Conversely, ORE1 interacts with PIFs to suppress
the chloroplast maintenance master regulators GOLDEN2-LIKE 1 (GLK1) and GLK2. This
antagonistic action of ORE1 on GLKs shifts the balance from chloroplast maintenance to
deterioration [88].
Apart from the ABA and ethylene signaling pathways, dark-induced leaf senescence
also involves the participation of JA. The genes responsible for JA biosynthesis, namely
lipoxygensase 2 (LOX2) and allene oxide synthase (AOS), are up-regulated during dark-
induced leaf senescence, and the application of exogenous JA expedites the senescence
process [
89
]. Overall, the induction of leaf senescence by dark treatment is governed by
an intricate network of molecular mechanisms encompassing various genes and regulatory
pathways. The identification of these pivotal genes and pathways offers valuable insights into
Int. J. Mol. Sci. 2023,24, 11996 7 of 17
the regulatory mechanisms underlying dark-induced leaf senescence and holds potential for
the development of strategies aimed at delaying or preventing leaf senescence in crop plants.
2.5. Low Oxygen-Induced Leaf Senescence
Low oxygen, also referred to as hypoxia, represents an abiotic stress condition capable
of triggering leaf senescence in plants [
90
92
]. In response to low oxygen levels, plants
activate various adaptive mechanisms to maintain cellular homeostasis and minimize
oxidative damage. However, prolonged exposure to hypoxia can accelerate leaf senescence,
leading to reduced plant growth and yield. Notably, leaf senescence is a prominent visible
symptom observed in plants subjected to extended submergence [
90
92
]. Chlorophyll
degradation initiates during the hypoxic phase and becomes evident after prolonged
submergence (typically lasting 5 to 7 days) in rice and Arabidopsis [9092].
At the molecular level, the regulation of hypoxia-induced leaf senescence involves
a complex interplay of genes and signaling pathways. Among the key contributors to
this process are the transcription factors belonging to the group VII ethylene response
factor (ERFVIIs), which stabilize under hypoxic conditions and activate downstream gene
expression to facilitate plant adaptation to low oxygen levels [
93
95
]. In rice, the ERFVII
transcription factor known as submergence 1a (SUB1A) functions as a regulator of submer-
gence tolerance by attenuating leaf senescence during prolonged submergence. Through
functional characterization, it was revealed that the induction of SUB1A expression during
submergence restricts further ethylene production and reduces gibberellic acid respon-
siveness. As a result, shoot tissues experience a decrease in carbohydrate consumption,
chlorophyll breakdown, amino acid accumulation, and elongation growth [
90
92
]. This
quiescence response to submergence aids in preserving carbohydrate reserves and the
capacity for photosynthesis. The prevention of carbohydrate depletion may contribute to
the milder manifestation of leaf senescence observed during submergence [96].
Interestingly, ectopic overexpression of SUB1A not only delays darkness-induced
leaf senescence but also limits ethylene production and responsiveness to JA and salicylic
acid (SA). This suppression of ethylene, JA, and SA signaling pathways results in the
preservation of chlorophyll and carbohydrates [
97
]. The delay in leaf senescence conferred
by SUB1A contributes to enhanced tolerance to submergence, drought, and oxidative
stress [
96
98
]. Collectively, the molecular mechanisms governing hypoxia-induced leaf
senescence are intricate and multifaceted. Gaining a comprehensive understanding of these
mechanisms is crucial for the development of strategies aimed at enhancing plant tolerance
to hypoxia and mitigating its adverse effects on plant growth and yield.
2.6. Extreme Temperatures Stress-Induced Leaf Senescence
Heat stress is one of the major environmental factors that trigger precocious senescence
in plans. Heat-stress-induced leaf senescence is associated with ethylene accumulation
and chlorophyll loss [
2
,
99
]. High-temperature treatment increased ethylene production
in soybean (Glycine max) leaves and pods, which may be due to higher ACC synthase
activity [
99
]. Pheophytinase (PPH) could be one of enzymes that play key roles in regulating
heat-accelerated chlorophyll degradation [
100
]. After heat stress, the survival rate of pph
mutant plants was significantly higher than that of wild type plants. It also led to a
significant decrease in chlorophyll content in wild type plants and pph mutants, but the
decrease was greater in wild type plants. The previously mentioned PIF4 and PIF5 are
key regulators of heat-induced senescence [
37
40
]. Under heat stress, leaf senescence was
delayed in pif4 and pif5 mutants and accelerated in transgenic lines compared with the wild
type. NAC019,SAG113, and IAA29 were characterized as direct targets of PIF4 and PIF5. In
addition, PIF4 and PIF5 proteins accumulate with the progression of heat stress-induced
leaf senescence and are regulate at the transcriptional and posttranscriptional levels [
101
].
In addition, mutation of premature senescence leaf 50 (PSL50) led to higher heat sensitivity,
reduced survival, excessive hydrogen peroxide (H
2
O
2
) content, and increased cell death
under heat stress in rice. This result suggests that PSL50 improves heat tolerance by
Int. J. Mol. Sci. 2023,24, 11996 8 of 17
regulating H
2
O
2
signaling under heat stress [
102
]. Low temperature and short day length
could result in the decrease in cytokinin and the increase in abscisic acid in leaf tissue, which
directly trigger/promote senescence [
103
], which was supported by another study [
104
]. So
far, low-temperature-induced leaf senescence has not been well-studied, and the underlying
molecular regulatory mechanisms remain to be explored.
2.7. Other Abiotic Stresses-Induced Leaf Senescence
Apart from the previously mentioned abiotic stresses, additional factors such as
extreme temperatures, high sugar levels, and UV radiation can also trigger premature leaf
senescence [
2
,
8
]. Elevated sugar levels within plant tissues lead to reduced photosynthesis
and early onset of senescence. The loss of hexokinase-1 (HXK1) function results in a delayed
senescence phenotype [
105
], whereas the overexpression of Arabidopsis HXK1 (AtHXK1) in
tomato plants accelerates senescence [
106
]. These findings indicate the involvement of the
sugar sensor HXK1 in sugar signaling during senescence. Intriguingly, the hxk/gin2 mutant
does not accumulate hexose in senescing leaves [
107
]. Moreover, the hxk/gin2 mutant
exhibits a delay in senescence induction by externally supplied glucose [
105
], suggesting
that HXK1 plays a role in sugar metabolism and response during senescence. Notably,
growth on glucose in combination with low nitrogen supply induces leaf yellowing and
alters gene expression patterns, characteristic of developmental senescence. Importantly,
the senescence-specific gene SAG12 is significantly upregulated by glucose. Additionally,
two senescence-associated MYB transcription factor genes, production of anthocyanin
pigment 1 (PAP1) and PAP2, are induced by glucose [
108
]. In Arabidopsis, glucose and
fructose accumulate substantially during leaf developmental senescence, while the sucrose
content remains relatively unchanged [
107
]. Generally, the sugar content in leaves gradually
increases, reaching its peak during the mature green stage or early senescence stages.
Although the mechanisms underlying the maintenance of carbon storage molecules, such
as sugars and starch, during senescence are not fully understood, sugars undoubtedly play
a crucial role in driving cellular processes in senescing leaves [109].
Moreover, the presence of heavy metal pollutants, such as cadmium, poses a significant
environmental challenge, leading to detrimental effects on plant growth and development.
Cadmium toxicity triggers the generation of ROS, disrupts the photosynthetic system, and
disrupts nutrient balance, ultimately accelerating leaf senescence [
110
,
111
]. Intriguingly,
the accumulation of cadmium in leaves increases exponentially during the senescence
process [
112
], indicating a clear association between leaf senescence and cadmium accu-
mulation. However, the exact mechanism of cadmium accumulation in senescing leaves
and the causal relationship between cadmium accumulation and senescence remain un-
clear. In particular, senescing leaves of tall fescue (Festuca arundinacea) can serve as a
means to remove cadmium from polluted soil through a sustainable approach known as
phytoextraction [110,112].
3. Improvement of Stress Tolerance through Regulation of Leaf Senescence
Understanding leaf senescence holds great importance due to its potential for im-
proving crop yield and quality. Manipulating the timing of leaf senescence enables plant
breeders to enhance photosynthetic efficiency, nutrient absorption, and stress tolerance,
leading to increased crop yield and improved quality. Additionally, leaf senescence plays a
pivotal role in plant adaptation to environmental stress. Exploring leaf senescence provides
valuable insights for developing stress-tolerant plants capable of withstanding adverse
conditions like drought, heat, or cold, thereby minimizing the detrimental effects of these
stressors on plant growth and productivity.
3.1. Utilization of Senescence-Specific or Stress-Associated Promoters
By utilizing the promoter of a senescence-specific gene SAG12, Gan and Amasino
designed an ingenious and elegant auto-regulatory senescence-inhibition system, pSAG12-
IPT [
25
] (Figure 1A). The promoter of SAG12 was linked to the coding region of the isopen-
Int. J. Mol. Sci. 2023,24, 11996 9 of 17
tenyltransferase gene (IPT), which regulates the rate-limiting step in cytokinin biosynthesis,
to form the chimeric gene pSAG12-IPT [
25
]. At the onset of senescence, this promoter acti-
vates IPT expression and increases cytokinin content to levels that prevent leaf senescence.
Repression of senescence in turn attenuates promoter expression to prevent overproduction
of cytokinin. The use of senescence promoters is essential to avoid premature IPT overex-
pression and CK hyper-production ahead of senescence. The auto-regulatory biosynthetic
system using pSAG12-IPT was proven to be an effective strategy for developing transgenic
plants to increase yield by delaying senescence and extending the shelf life of isolated
organs such as leaves, flowers, and fruits [
28
]. The pSAG12-IPT system had been widely
used in numerous plant species [
28
], including wheat (Triticum aestivum L.) [
113
], alfalfa
(Medicago sativa) [
114
], lettuce (Lactuca sativa L. cv Evola) [
115
], cassava (Manihot esculenta
Crantz) [
27
], and creeping bentgrass (Agrostis stolonifera L. ‘Penncross’) [
116
], etc. However,
it should be noted that the pSAG12-IPT system possibly directly or indirectly affects plant
development, including delayed flowering in transgenic lettuce [
115
], and reduced nitro-
gen accumulation in young leaves by altering sink-source relationships in tobacco [
117
].
To achieve maximum effectiveness, practical applications should carefully consider the
advantages and disadvantages of this system.
Int. J. Mol. Sci. 2023, 24, x FOR PEER REVIEW 10 of 17
proved turf quality, photochemical efficiency, chlorophyll content, relative leaf water con-
tent, and root-to-stem ratio. Furthermore, transgenic poplar lines expressing IPT under
the control of the promoter of PtRD26 (PtRD26pro-IPT) (Figure 1F), a senescence and
drought-inducible NAC transcription factor in poplar, displayed various phenotypic im-
provements, including enhanced growth and drought tolerance [120].
Another type of experimental design is to use promoters of SAG12 to drive the ex-
pression of different genes. For example, tobacco plants overexpressing the maize home-
obox gene knotted1 (kn1) under the driver of SAG12 promoter, designated as pSAG12-kn1,
exhibited a significant delay in leaf senescence, with an increase in chlorophyll content
and a decrease in the number of dead leaves. In the detached leaves of pSAG12-kn1 plants,
senescence was also postponed [121]. Collectively, these studies provided the possibility
of regulating the onset of leaf senescence by cleverly using senescence and stress-related
gene promoters to drive the expression of IPT and developmental genes, thereby improv-
ing crop resistance, yield, and quality.
Figure 1. The diagrams show pSAG12-IPT and its various variants. (A) The auto-regulatory senes-
cence-inhibition system of pSAG12-IPT [25]. (BF) A range of variants have been developed based
on the design concept of pSAG12-IPT, including (B) pSARK-IPT [26], (C) AtMYB32xs-IPT (Red rec-
tangle represent the deleted root motif of 360bp in promoter) [118], (D) COR15A-IPT [119], (E)
HSP18.2-IPT [116], and (F) PtRD26pro-IPT [120]. The yellow parts represent the senescence-specific
promoters. The dark green part represents the developmental process-related promoter. The blue
part represents the cold-induced promoter. The red part represents the heat shock promoter.
3.2. Modulation of Expression of Senescence Associated Genes
An alternative approach to influencing the leaf senescence process involves manipu-
lating the expression of crucial senescence genes, with the aim of enhancing crop re-
sistance and yield. For instance, the knockout of OsNAP, a rice ortholog of
ANAC029/AtNAP [122], resulted in prolonged grain-filling periods and increased grain
yields compared to the wild type [123]. Therefore, precise regulation of OsNAP expression
holds promise for improving stress resistance in rice. A noteworthy discovery is the po-
tential use of naturally occurring Stay-Green (OsSGR) promoter and associated longevity
variants in breeding programs to enhance rice yield [124]. Nam and colleagues conducted
quantitative trait loci (QTL) mapping and identified genetic differences in life cycle and
senescence patterns between two rice subspecies, indica, and japonica [124]. They found
that promoter variations in the OsSGR gene, which encodes the chlorophyll-degrading
Figure 1.
The diagrams show pSAG12-IPT and its various variants. (
A
) The auto-regulatory
senescence-inhibition system of pSAG12-IPT [
25
]. (
B
F
) A range of variants have been developed
based on the design concept of pSAG12-IPT, including (
B
)pSARK-IPT [
26
], (
C
)AtMYB32xs-IPT
(Red rectangle represent the deleted root motif of 360bp in promoter) [
118
], (
D
)COR15A-IPT [
119
],
(
E
) HSP18.2-IPT [
116
], and (
F
)PtRD26
pro
-IPT [
120
]. The yellow parts represent the senescence-specific
promoters. The dark green part represents the developmental process-related promoter. The blue
part represents the cold-induced promoter. The red part represents the heat shock promoter.
A range of variants were developed based on the design concept of pSAG12-IPT.
One approach involves utilizing different promoters to control the expression of IPT. For
instance, a modified version of this cytokinin (CK) auto-regulatory cycle strategy em-
ployed the promoter of senescence-associated receptor kinase (SARK) fused with the IPT gene
(Figure 1B). Transgenic tobacco plants carrying pSARK-IPT exhibited enhanced survival un-
der severe drought conditions, accompanied by improvements in photosynthetic rate and
water use efficiency [26]. In these plants, the activation of the SARK promoter in response
to drought-induced leaf senescence led to delayed senescence through cytokinin biosynthe-
sis. However, it should be noted that premature activation of leaf senescence may occur
during drought, and the benefits in terms of yield increase may not be realized under well-
watered conditions when using stress-inducible promoters. To address the issues of stress
inducibility and proper regulation of IPT genes, Spangenberg and colleagues ingeniously
Int. J. Mol. Sci. 2023,24, 11996 10 of 17
employed a modified promoter derived from the developmental process-related gene
AtMYB32 (AtMYB32xs) (Figure 1C), which removed the 360 bp root-specific motif [
118
].
Stable transgenic oilseed rape (Brassica napus) plants expressing AtMYB32xs-IPT exhibited
delayed leaf senescence under controlled environment and field conditions. Remarkably,
these AtMYB32xs-IPT plants achieved significantly higher seed yield during both rainy
seasons and field irrigation conditions [
118
]. In petunia and chrysanthemum, transgenic
plants known as COR15A-IPT were generated using the cold induction promoter from the
cold-regulated15a (COR15A) gene of Arabidopsis thaliana (Figure 1D) [
119
]. Intriguingly,
COR15A-IPT plants and their detached leaves remained green and healthy during extended
dark storage (4 weeks at 25
C) following an initial exposure to a brief period of cold induc-
tion (72 h at 4
C). This study presented an approach to prolong the lifespan of transplants
or excised leaves during storage under dark and cold conditions, which is particularly
beneficial for long-distance transport. The heat shock promoter HSP18.2 was fused with
IPT to generate HSP18.2-IPT transgenic plants in creeping bentgrass (Agrostis stolonifera)
(Figure 1E) [
116
]. The HSP18.2-IPT transgenic lines exhibited significantly improved turf
quality, photochemical efficiency, chlorophyll content, relative leaf water content, and
root-to-stem ratio. Furthermore, transgenic poplar lines expressing IPT under the control of
the promoter of PtRD26 (PtRD26
pro
-IPT) (Figure 1F), a senescence and drought-inducible
NAC transcription factor in poplar, displayed various phenotypic improvements, including
enhanced growth and drought tolerance [120].
Another type of experimental design is to use promoters of SAG12 to drive the expres-
sion of different genes. For example, tobacco plants overexpressing the maize homeobox
gene knotted1 (kn1) under the driver of SAG12 promoter, designated as pSAG12-kn1, ex-
hibited a significant delay in leaf senescence, with an increase in chlorophyll content and
a decrease in the number of dead leaves. In the detached leaves of pSAG12-kn1 plants,
senescence was also postponed [
121
]. Collectively, these studies provided the possibility of
regulating the onset of leaf senescence by cleverly using senescence and stress-related gene
promoters to drive the expression of IPT and developmental genes, thereby improving crop
resistance, yield, and quality.
3.2. Modulation of Expression of Senescence Associated Genes
An alternative approach to influencing the leaf senescence process involves manipu-
lating the expression of crucial senescence genes, with the aim of enhancing crop resistance
and yield. For instance, the knockout of OsNAP, a rice ortholog of ANAC029/AtNAP [
122
],
resulted in prolonged grain-filling periods and increased grain yields compared to the wild
type [
123
]. Therefore, precise regulation of OsNAP expression holds promise for improving
stress resistance in rice. A noteworthy discovery is the potential use of naturally occurring
Stay-Green (OsSGR) promoter and associated longevity variants in breeding programs
to enhance rice yield [
124
]. Nam and colleagues conducted quantitative trait loci (QTL)
mapping and identified genetic differences in life cycle and senescence patterns between
two rice subspecies, indica, and japonica [
124
]. They found that promoter variations in
the OsSGR gene, which encodes the chlorophyll-degrading Mg
++
-dechelatase, triggered
earlier and higher induction of OsSGR in indica, thereby accelerating senescence in indica
cultivars. Introducing the japonica OsSGR allele into indica-type cultivars resulted in de-
layed senescence, increased grain yield, and improved photosynthetic capacity. This study
highlighted the potential of modifying the senescence-related promoter region, in addition
to gene coding regions, to achieve delayed leaf senescence and increased yield. The use of
gene editing technologies like CRISPR/Cas9 offers a powerful tool for manipulating key
genes involved in regulating leaf senescence, and further research is necessary to identify
and manipulate additional genes involved in these processes [8].
To summarize, comprehending the molecular regulatory mechanisms underlying leaf
senescence holds the potential to inform the development of molecular breeding strategies
aimed at enhancing plant tolerance to abiotic stresses, increasing grain yield, and improving
crop quality. A significant objective in leaf senescence research is the cultivation of plants
Int. J. Mol. Sci. 2023,24, 11996 11 of 17
with ideal leaf senescence phenotype (PILSP). PILSP exhibit the remarkable ability to
effectively coordinate growth and stress tolerance, integrate both internal and external
signals, and initiate leaf senescence at the optimal time. In the case of annual plants,
leaves remain green in the initial stages of plant growth, resisting internal and external
stresses, and only enter senescence when the leaves die, allowing for the complete transfer
of photosynthetic products to the seeds. In contrast, perennial plants retain their leaves
even under environmental stresses, and upon stress removal, leaf function is promptly
restored. Consequently, when the leaves eventually die, the photosynthetic products can
be fully channeled to the main stem or the growing organ.
4. Prospects
In recent years, considerable advancements have been made in leaf senescence re-
search; however, several challenges remain in fully comprehending the molecular mech-
anisms of leaf senescence and effectively applying this knowledge to enhance crop im-
provement. One of the foremost challenges lies in the intricate nature of the regulatory
network governing leaf senescence, posing difficulties in identifying pivotal genes and
regulatory pathways. Additionally, the complexity is compounded by the fact that diverse
environmental factors, such as drought, high temperature, and nutrient deficiency, can
trigger leaf senescence through distinct pathways, further adding to the intricacy of the
regulatory network.
To overcome these challenges, several strategies have been proposed. Firstly, a com-
prehensive analysis of the leaf senescence regulatory network and the identification of key
genes and regulatory pathways can be achieved through the integration of multi-omics ap-
proaches, including genomics, transcriptomics, proteomics, and metabolomics [
19
,
125
127
].
These approaches enable a holistic understanding of the complex mechanisms involved.
Secondly, advanced imaging techniques, such as live imaging and high-resolution mi-
croscopy, offer the opportunity to monitor the dynamic progression of leaf senescence
and visualize the molecular events at play. For instance, confocal imaging fluorometer
allows high spatio-temporal-resolution detection of chlorophyll fluorescence dynamics
at the single chloroplast level [
128
]. Additionally, the combination of high-speed three-
dimensional laser scanning confocal microscopy and high-sensitivity multiple-channel
detection facilitates in-depth investigations of the spatial and temporal dynamics of chloro-
plast degradation during leaf senescence [
129
]. Thirdly, genetic engineering techniques,
particularly CRISPR/Cas9-mediated genome editing, provide a means to manipulate the
expression of key senescence-related genes and elucidate their roles in the process. A
recent study successfully employed CRISPR/Cas9-mediated knockout to demonstrate the
regulatory function of the peptide hormone CLE42 in leaf senescence [130].
In conclusion, leaf senescence research holds immense potential for enhancing crop
yield and quality. However, addressing the existing challenges is crucial. By harnessing
the power of multi-omics approaches, advanced imaging techniques, and genetic engineer-
ing, we can gain a deeper understanding of the molecular mechanisms underlying leaf
senescence and effectively apply this knowledge to drive crop improvement.
Author Contributions:
Conceptualization, Z.L.; writing—original draft preparation, S.T. and Y.S.;
writing—reviewing and editing, S.T., Y.S., L.S. and Z.L.; supervision, Z.L. All authors have read and
agreed to the published version of the manuscript.
Funding:
This research was funded by Beijing Municipal Natural Science Foundation (5232015 to Z.L.),
the Open Research Fund of the National Center for Protein Sciences at Peking University in Beijing
(KF-202304), the National Natural Science Foundation of China (32170345, 31970196, and 32011540381
to Z.L.), and the High-level Talent Introduction Programme of Beijing Forestry University.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Int. J. Mol. Sci. 2023,24, 11996 12 of 17
Data Availability Statement:
No new data were created or analyzed in this study. Data sharing is
not applicable to this article.
Acknowledgments:
We sincerely apologize to all those authors whose work is not included in this
review paper due to space limitations.
Conflicts of Interest: The authors declare no conflict of interest.
Abbreviations
ROS Reactive Oxygen Species
SAG Senescence-Associated Gene
NLA Nitrogen Limitation Adaptation
PHO2 PHOSPHATE2
UBC Ubiquitin-conjugating enzyme
UBP12 Ubiquitin-specific protease 12
GDS1 GROWTH, DEVELOPMENT AND SPLICING 1
ORE1 ORESARA1
JUB1 JUNGBRUNNEN1
ERF ETHYLENE RESPONSE FACTOR
COR15A COLD-REGULATED15A
ERD10 EARLY RESPONSIVE TO DEHYDRATION10
RD29A RESPONSIVE TO DESICCATION29A
PIF PHYTOCHROME-INTERACTING FACTOR
bZIP basic LEUCINE ZIPPER
IDL Individually Darkened Leaf
ABI5 ABSCISIC ACID INSENSITIVE 5
EEL ENHANCED EM LEVELS
SGR1 STAYGREEN 1
NYC1 NON-YELLOW COLORING 1
GDL1 GOLDEN2-LIKE 1
LOX2 LIPOXYGENASE 2
AOS ALLENE OXIDE SYNTHASE
SUB1A SUBMERGENCE1A
HXK1 Hexokinase-1
PAP1 PRODUCTION OF ANTHOCYANIN PIGMENT 1
IPT Isopentenyltransferase
SARK Senescence-associated Receptor Kinase
Kn1 Knotted1
QTL Quantitative Trait Loci
PILSP Plants with Ideal Leaf Senescence Phenotype
ROS Reactive Oxygen Species
SAG Senescence-Associated Gene
NLA Nitrogen Limitation Adaptation
PHO2 PHOSPHATE2
UBC Ubiquitin-conjugating enzyme
UBP12 Ubiquitin-specific protease 12
GDS1 GROWTH, DEVELOPMENT AND SPLICING 1
ORE1 ORESARA1
JUB1 JUNGBRUNNEN1
ERF ETHYLENE RESPONSE FACTOR
COR15A COLD-REGULATED15A
ERD10 EARLY RESPONSIVE TO DEHYDRATION10
References
1. Guo, Y.; Gan, S. Leaf senescence: Signals, execution, and regulation. Curr. Top. Dev. Biol. 2005,71, 83–112.
2. Lim, P.O.; Kim, H.J.; Nam, H.G. Leaf senescence. Annu. Rev. Plant Biol. 2007,58, 115–136. [CrossRef]
Int. J. Mol. Sci. 2023,24, 11996 13 of 17
3.
Wang, H.L.; Zhang, Y.; Wang, T.; Yang, Q.; Yang, Y.; Li, Z.; Li, B.; Wen, X.; Li, W.; Yin, W.; et al. An alternative splicing variant
of PtRD26 delays leaf senescence by regulating multiple NAC transcription factors in Populus. Plant Cell
2021
,33, 1594–1614.
[CrossRef]
4.
Keskitalo, J.; Bergquist, G.; Gardestrom, P.; Jansson, S. A cellular timetable of autumn senescence. Plant Physiol.
2005
,139,
1635–1648. [CrossRef] [PubMed]
5.
Cooke, J.E.; Weih, M. Nitrogen storage and seasonal nitrogen cycling in Populus: Bridging molecular physiology and ecophysiol-
ogy. New Phytol. 2005,167, 19–30. [CrossRef] [PubMed]
6.
Andleeb, T.; Knight, E.; Borrill, P. Wheat NAM genes regulate the majority of early monocarpic senescence transcriptional changes
including nitrogen remobilization genes. G3 2023,13, jkac275. [CrossRef]
7.
Wei, S.; Li, X.; Lu, Z.; Zhang, H.; Ye, X.; Zhou, Y.; Li, J.; Yan, Y.; Pei, H.; Duan, F.; et al. A transcriptional regulator that boosts grain
yields and shortens the growth duration of rice. Science 2022,377, eabi8455. [CrossRef] [PubMed]
8.
Guo, Y.; Ren, G.; Zhang, K.; Li, Z.; Miao, Y.; Guo, H. Leaf senescence: Progression, regulation, and application. Mol. Hortic.
2021
,
1, 5. [CrossRef]
9.
Cao, J.; Zhang, Y.; Tan, S.; Yang, Q.; Wang, H.-L.; Xia, X.; Luo, J.; Guo, H.; Zhang, Z.; Li, Z. LSD 4.0: An improved database for
comparative studies of leaf senescence. Mol. Hortic. 2022,2, 24. [CrossRef]
10.
Cao, J.; Liu, H.; Tan, S.; Li, Z. Transcription Factors-Regulated Leaf Senescence: Current Knowledge, Challenges and Approaches.
Int. J. Mol. Sci. 2023,24, 9245. [CrossRef]
11.
Moschen, S.; Di Rienzo, J.A.; Higgins, J.; Tohge, T.; Watanabe, M.; Gonzalez, S.; Rivarola, M.; Garcia-Garcia, F.; Dopazo, J.;
Hopp, H.E.; et al.
Integration of transcriptomic and metabolic data reveals hub transcription factors involved in drought stress
response in sunflower (Helianthus annuus L.). Plant Mol. Biol. 2017,94, 549–564. [CrossRef] [PubMed]
12.
Moschen, S.; Bengoa Luoni, S.; Paniego, N.B.; Hopp, H.E.; Dosio, G.A.; Fernandez, P.; Heinz, R.A. Identification of candidate
genes associated with leaf senescence in cultivated sunflower (Helianthus annuus L.). PLoS ONE
2014
,9, e104379. [CrossRef]
[PubMed]
13.
Trupkin, S.A.; Astigueta, F.H.; Baigorria, A.H.; Garcia, M.N.; Delfosse, V.C.; Gonzalez, S.A.; Perez de la Torre, M.C.; Moschen, S.;
Lia, V.V.; Fernandez, P.; et al. Identification and expression analysis of NAC transcription factors potentially involved in leaf and
petal senescence in Petunia hybrida.Plant Sci. 2019,287, 110195. [CrossRef] [PubMed]
14.
Li, Z.; Peng, J.; Wen, X.; Guo, H. Ethylene-insensitive3 is a senescence-associated gene that accelerates age-dependent leaf
senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell 2013,25, 3311–3328. [CrossRef] [PubMed]
15.
Miao, Y.; Laun, T.; Zimmermann, P.; Zentgraf, U. Targets of the WRKY53 transcription factor and its role during leaf senescence in
Arabidopsis. Plant Mol. Biol. 2004,55, 853–867. [CrossRef] [PubMed]
16.
Wang, Q.; Li, X.; Guo, C.; Wen, L.; Deng, Z.; Zhang, Z.; Li, W.; Liu, T.; Guo, Y. Senescence-Related Receptor Kinase 1 (SENRK1)
functions downstream of WRKY53 in regulating leaf senescence in Arabidopsis. J. Exp. Bot. 2023. [CrossRef] [PubMed]
17. Sakuraba, Y.; Kim, D.; Paek, N.C. Salt Treatments and Induction of Senescence. Methods Mol. Biol. 2018,1744, 141–149.
18.
Sade, N.; Del Mar Rubio-Wilhelmi, M.; Umnajkitikorn, K.; Blumwald, E. Stress-induced senescence and plant tolerance to abiotic
stress. J. Exp. Bot. 2018,69, 845–853. [CrossRef]
19.
Woo, H.R.; Kim, H.J.; Lim, P.O.; Nam, H.G. Leaf Senescence: Systems and Dynamics Aspects. Annu. Rev. Plant Biol.
2019
,70,
347–376. [CrossRef]
20.
Li, Z.; Kim, J.H.; Kim, J.; Lyu, J.I.; Zhang, Y.; Guo, H.; Nam, H.G.; Woo, H.R. ATM suppresses leaf senescence triggered by DNA
double-strand break through epigenetic control of senescence-associated genes in Arabidopsis. New Phytol.
2020
,227, 473–484.
[CrossRef]
21.
Han, D.; Du, M.; Zhou, Z.; Wang, S.; Li, T.; Han, J.; Xu, T.; Yang, G. Overexpression of a Malus baccata NAC Transcription Factor
Gene MbNAC25 Increases Cold and Salinity Tolerance in Arabidopsis. Int. J. Mol. Sci. 2020,21, 1198. [CrossRef] [PubMed]
22.
Hu, D.G.; Sun, C.H.; Zhang, Q.Y.; Gu, K.D.; Hao, Y.J. The basic helix-loop-helix transcription factor MdbHLH3 modulates leaf
senescence in apple via the regulation of dehydratase-enolase-phosphatase complex 1. Hortic. Res.
2020
,7, 50. [CrossRef]
[PubMed]
23.
Lira, B.S.; Gramegna, G.; Trench, B.A.; Alves, F.R.R.; Silva, E.M.; Silva, G.F.F.; Thirumalaikumar, V.P.; Lupi, A.C.D.; Demarco, D.;
Purgatto, E.; et al. Manipulation of a Senescence-Associated Gene Improves Fleshy Fruit Yield. Plant Physiol.
2017
,175, 77–91.
[CrossRef]
24.
Ma, X.; Zhang, Y.; Tureckova, V.; Xue, G.P.; Fernie, A.R.; Mueller-Roeber, B.; Balazadeh, S. The NAC Transcription Factor SlNAP2
Regulates Leaf Senescence and Fruit Yield in Tomato. Plant Physiol. 2018,177, 1286–1302. [CrossRef]
25.
Gan, S.; Amasino, R.M. Inhibition of leaf senescence by autoregulated production of cytokinin. Science
1995
,270, 1986–1988.
[CrossRef]
26.
Rivero, R.M.; Kojima, M.; Gepstein, A.; Sakakibara, H.; Mittler, R.; Gepstein, S.; Blumwald, E. Delayed leaf senescence induces
extreme drought tolerance in a flowering plant. Proc. Natl. Acad. Sci. USA 2007,104, 19631–19636. [CrossRef]
27.
Zhang, P.; Wang, W.Q.; Zhang, G.L.; Kaminek, M.; Dobrev, P.; Xu, J.; Gruissem, W. Senescence-inducible expression of isopentenyl
transferase extends leaf life, increases drought stress resistance and alters cytokinin metabolism in cassava. J. Integr. Plant Biol.
2010,52, 653–669. [CrossRef]
28.
Guo, Y.; Gan, S.S. Translational researches on leaf senescence for enhancing plant productivity and quality. J. Exp. Bot.
2014
,65,
3901–3913. [CrossRef]
Int. J. Mol. Sci. 2023,24, 11996 14 of 17
29.
Park, B.S.; Yao, T.; Seo, J.S.; Wong, E.C.C.; Mitsuda, N.; Huang, C.H.; Chua, N.H. Arabidopsis NITROGEN LIMITATION
ADAPTATION regulates ORE1 homeostasis during senescence induced by nitrogen deficiency. Nat. Plants
2018
,4, 898–903.
[CrossRef] [PubMed]
30.
Park, S.H.; Jeong, J.S.; Seo, J.S.; Park, B.S.; Chua, N.H. Arabidopsis ubiquitin-specific proteases UBP12 and UBP13 shape ORE1
levels during leaf senescence induced by nitrogen deficiency. New Phytol. 2019,223, 1447–1460. [CrossRef]
31.
Fan, H.; Quan, S.; Ye, Q.; Zhang, L.; Liu, W.; Zhu, N.; Zhang, X.; Ruan, W.; Yi, K.; Crawford, N.M.; et al. A molecular framework
underlying low-nitrogen-induced early leaf senescence in Arabidopsis thaliana.Mol. Plant
2023
,16, 756–774. [CrossRef] [PubMed]
32.
Peng, M.; Hannam, C.; Gu, H.; Bi, Y.M.; Rothstein, S.J. A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts
the adaptability of Arabidopsis to nitrogen limitation. Plant J. 2007,50, 320–337. [CrossRef]
33.
Liu, W.; Sun, Q.; Wang, K.; Du, Q.; Li, W.X. Nitrogen Limitation Adaptation (NLA) is involved in source-to-sink remobilization of
nitrate by mediating the degradation of NRT1.7 in Arabidopsis. New Phytol. 2017,214, 734–744. [CrossRef] [PubMed]
34.
Delhaize, E.; Randall, P.J. Characterization of a Phosphate-Accumulator Mutant of Arabidopsis thaliana. Plant Physiol.
1995
,107,
207–213. [CrossRef] [PubMed]
35.
Dong, B.; Rengel, Z.; Delhaize, E. Uptake and translocation of phosphate by pho2 mutant and wild-type seedlings of Arabidopsis
thaliana. Planta 1998,205, 251–256. [CrossRef]
36.
Kim, D.W.; Jeon, S.J.; Hwang, S.M.; Hong, J.C.; Bahk, J.D. The C3H-type zinc finger protein GDS1/C3H42 is a nuclear-speckle-
localized protein that is essential for normal growth and development in Arabidopsis. Plant Sci. 2016,250, 141–153. [CrossRef]
37.
Liebsch, D.; Keech, O. Dark-induced leaf senescence: New insights into a complex light-dependent regulatory pathway. New
Phytol. 2016,212, 563–570. [CrossRef]
38.
Song, Y.; Yang, C.; Gao, S.; Zhang, W.; Li, L.; Kuai, B. Age-triggered and dark-induced leaf senescence require the bHLH
transcription factors PIF3, 4, and 5. Mol. Plant 2014,7, 1776–1787. [CrossRef]
39.
Li, N.; Bo, C.; Zhang, Y.; Wang, L. Phytochrome Interacting Factors PIF4 and PIF5 promote heat stress induced leaf senescence in
Arabidopsis. J. Exp. Bot. 2021,72, 4577–4589. [CrossRef] [PubMed]
40.
Sakuraba, Y.; Jeong, J.; Kang, M.Y.; Kim, J.; Paek, N.C.; Choi, G. Phytochrome-interacting transcription factors PIF4 and PIF5
induce leaf senescence in Arabidopsis. Nat. Commun. 2014,5, 4636. [CrossRef] [PubMed]
41. Zhang, H.; Zhu, J.; Gong, Z.; Zhu, J.K. Abiotic stress responses in plants. Nat. Rev. Genet. 2022,23, 104–119. [CrossRef]
42.
Munne-Bosch, S.; Alegre, L. Die and let live: Leaf senescence contributes to plant survival under drought stress. Funct. Plant Biol.
2004,31, 203–216. [CrossRef] [PubMed]
43.
Lee, S.; Seo, P.J.; Lee, H.J.; Park, C.M. A NAC transcription factor NTL4 promotes reactive oxygen species production during
drought-induced leaf senescence in Arabidopsis. Plant J. 2012,70, 831–844. [CrossRef] [PubMed]
44.
Hickman, R.; Hill, C.; Penfold, C.A.; Breeze, E.; Bowden, L.; Moore, J.D.; Zhang, P.; Jackson, A.; Cooke, E.; Bewicke-Copley, F.;
et al. A local regulatory network around three NAC transcription factors in stress responses and senescence in Arabidopsis leaves.
Plant J. 2013,75, 26–39. [CrossRef] [PubMed]
45.
Zhao, Y.; Chan, Z.; Gao, J.; Xing, L.; Cao, M.; Yu, C.; Hu, Y.; You, J.; Shi, H.; Zhu, Y.; et al. ABA receptor PYL9 promotes drought
resistance and leaf senescence. Proc. Natl. Acad. Sci. USA 2016,113, 1949–1954. [CrossRef]
46.
Claeys, H.; Inze, D. The agony of choice: How plants balance growth and survival under water-limiting conditions. Plant Physiol.
2013,162, 1768–1779. [CrossRef]
47.
Athar, H.U.; Zulfiqar, F.; Moosa, A.; Ashraf, M.; Zafar, Z.U.; Zhang, L.; Ahmed, N.; Kalaji, H.M.; Nafees, M.; Hossain, M.A.; et al.
Salt stress proteins in plants: An overview. Front. Plant Sci. 2022,13, 999058. [CrossRef]
48.
Zulfiqar, F.; Ashraf, M. Nanoparticles potentially mediate salt stress tolerance in plants. Plant Physiol. Biochem.
2021
,160, 257–268.
[CrossRef]
49. Munns, R.; Tester, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 2008,59, 651–681. [CrossRef] [PubMed]
50. van Zelm, E.; Zhang, Y.; Testerink, C. Salt Tolerance Mechanisms of Plants. Annu. Rev. Plant Biol. 2020,71, 403–433. [CrossRef]
51.
Deinlein, U.; Stephan, A.B.; Horie, T.; Luo, W.; Xu, G.; Schroeder, J.I. Plant salt-tolerance mechanisms. Trends Plant Sci.
2014
,19,
371–379. [CrossRef]
52.
Fricke, W. Energy costs of salinity tolerance in crop plants: Night-time transpiration and growth. New Phytol.
2020
,225, 1152–1165.
[CrossRef]
53.
Munns, R.; Day, D.A.; Fricke, W.; Watt, M.; Arsova, B.; Barkla, B.J.; Bose, J.; Byrt, C.S.; Chen, Z.H.; Foster, K.J.; et al. Energy costs
of salt tolerance in crop plants. New Phytol. 2020,225, 1072–1090. [CrossRef]
54.
Tyerman, S.D.; Munns, R.; Fricke, W.; Arsova, B.; Barkla, B.J.; Bose, J.; Bramley, H.; Byrt, C.; Chen, Z.; Colmer, T.D.; et al. Energy
costs of salinity tolerance in crop plants. New Phytol. 2019,221, 25–29. [CrossRef]
55.
Kim, H.J.; Nam, H.G.; Lim, P.O. Regulatory network of NAC transcription factors in leaf senescence. Curr. Opin. Plant Biol.
2016
,
33, 48–56. [CrossRef]
56.
Park, S.J.; Park, S.; Kim, Y.; Hyeon, D.Y.; Park, H.; Jeong, J.; Jeong, U.; Yoon, Y.S.; You, D.; Kwak, J.; et al. Ethylene responsive
factor34 mediates stress-induced leaf senescence by regulating salt stress-responsive genes. Plant Cell Environ.
2022
,45, 1719–1733.
[CrossRef]
57.
Balazadeh, S.; Siddiqui, H.; Allu, A.D.; Matallana-Ramirez, L.P.; Caldana, C.; Mehrnia, M.; Zanor, M.I.; Kohler, B.;
Mueller-Roeber, B.
A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1
during salt-promoted senescence. Plant J. 2010,62, 250–264. [CrossRef]
Int. J. Mol. Sci. 2023,24, 11996 15 of 17
58.
Peng, J.; Li, Z.; Wen, X.; Li, W.; Shi, H.; Yang, L.; Zhu, H.; Guo, H. Salt-induced stabilization of EIN3/EIL1 confers salinity
tolerance by deterring ROS accumulation in Arabidopsis. PLoS Genet. 2014,10, e1004664. [CrossRef]
59.
Kim, Y.S.; Sakuraba, Y.; Han, S.H.; Yoo, S.C.; Paek, N.C. Mutation of the Arabidopsis NAC016 transcription factor delays leaf
senescence. Plant Cell Physiol. 2013,54, 1660–1672. [CrossRef]
60. Mahmood, K.; Xu, Z.; El-Kereamy, A.; Casaretto, J.A.; Rothstein, S.J. The Arabidopsis Transcription Factor ANAC032 Represses
Anthocyanin Biosynthesis in Response to High Sucrose and Oxidative and Abiotic Stresses. Front. Plant Sci.
2016
,7, 1548.
[CrossRef]
61.
Mahmood, K.; El-Kereamy, A.; Kim, S.H.; Nambara, E.; Rothstein, S.J. ANAC032 Positively Regulates Age-Dependent and
Stress-Induced Senescence in Arabidopsis thaliana. Plant Cell Physiol. 2016,57, 2029–2046. [CrossRef]
62.
Mito, T.; Seki, M.; Shinozaki, K.; Ohme-Takagi, M.; Matsui, K. Generation of chimeric repressors that confer salt tolerance in
Arabidopsis and rice. Plant Biotechnol. J. 2011,9, 736–746. [CrossRef]
63.
Yang, S.D.; Seo, P.J.; Yoon, H.K.; Park, C.M. The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into
leaf senescence via the COR/RD genes. Plant Cell 2011,23, 2155–2168. [CrossRef]
64.
Wu, A.; Allu, A.D.; Garapati, P.; Siddiqui, H.; Dortay, H.; Zanor, M.I.; Asensi-Fabado, M.A.; Munne-Bosch, S.; Antonio,
C.;
Tohge, T.; et al.
JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in
Arabidopsis. Plant Cell 2012,24, 482–506. [CrossRef]
65.
Podzimska-Sroka, D.; O’Shea, C.; Gregersen, P.L.; Skriver, K. NAC Transcription Factors in Senescence: From Molecular Structure
to Function in Crops. Plants 2015,4, 412–448. [CrossRef]
66.
Zhou, Y.; Huang, W.; Liu, L.; Chen, T.; Zhou, F.; Lin, Y. Identification and functional characterization of a rice NAC gene involved
in the regulation of leaf senescence. BMC Plant Biol. 2013,13, 132. [CrossRef]
67.
Zhao, D.; Derkx, A.P.; Liu, D.C.; Buchner, P.; Hawkesford, M.J. Overexpression of a NAC transcription factor delays leaf
senescence and increases grain nitrogen concentration in wheat. Plant Biol. 2015,17, 904–913. [CrossRef]
68.
Liu, G.; Li, X.; Jin, S.; Liu, X.; Zhu, L.; Nie, Y.; Zhang, X. Overexpression of rice NAC gene SNAC1 improves drought and
salt tolerance by enhancing root development and reducing transpiration rate in transgenic cotton. PLoS ONE
2014
,9, e86895.
[CrossRef]
69. Sakuraba, Y.; Piao, W.; Lim, J.H.; Han, S.H.; Kim, Y.S.; An, G.; Paek, N.C. Rice ONAC106 Inhibits Leaf Senescence and Increases
Salt Tolerance and Tiller Angle. Plant Cell Physiol. 2015,56, 2325–2339. [CrossRef]
70.
Liu, H.; Zhou, Y.; Li, H.; Wang, T.; Zhang, J.; Ouyang, B.; Ye, Z. Molecular and functional characterization of ShNAC1, an NAC
transcription factor from Solanum habrochaites. Plant Sci. 2018,271, 9–19. [CrossRef]
71.
Lu, X.; Zhang, X.; Duan, H.; Lian, C.; Liu, C.; Yin, W.; Xia, X. Three stress-responsive NAC transcription factors from Populus
euphratica differentially regulate salt and drought tolerance in transgenic plants. Physiol. Plant.
2018
,162, 73–97. [CrossRef]
[PubMed]
72.
Li, Z.; Zhang, Y.; Zou, D.; Zhao, Y.; Wang, H.L.; Zhang, Y.; Xia, X.; Luo, J.; Guo, H.; Zhang, Z. LSD 3.0: A comprehensive resource
for the leaf senescence research community. Nucleic Acids Res. 2020,48, D1069–D1075. [CrossRef] [PubMed]
73.
Zeng, D.D.; Yang, C.C.; Qin, R.; Alamin, M.; Yue, E.K.; Jin, X.L.; Shi, C.H. A guanine insert in OsBBS1 leads to early leaf senescence
and salt stress sensitivity in rice (Oryza sativa L.). Plant Cell Rep. 2018,37, 933–946. [CrossRef] [PubMed]
74.
Zhu, K.; Tao, H.; Xu, S.; Li, K.; Zafar, S.; Cao, W.; Yang, Y. Overexpression of salt-induced protein (salT) delays leaf senescence in
rice. Genet. Mol. Biol. 2019,42, 80–86. [CrossRef]
75.
Allu, A.D.; Soja, A.M.; Wu, A.; Szymanski, J.; Balazadeh, S. Salt stress and senescence: Identification of cross-talk regulatory
components. J. Exp. Bot. 2014,65, 3993–4008. [CrossRef]
76.
de Wit, M.; Galvao, V.C.; Fankhauser, C. Light-Mediated Hormonal Regulation of Plant Growth and Development. Annu. Rev.
Plant Biol. 2016,67, 513–537. [CrossRef]
77.
Weaver, L.M.; Amasino, R.M. Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened
plants. Plant Physiol. 2001,127, 876–886. [CrossRef]
78. Li, Z.; Zhao, T.; Liu, J.; Li, H.; Liu, B. Shade-Induced Leaf Senescence in Plants. Plants 2023,12, 1550. [CrossRef]
79.
Brouwer, B.; Ziolkowska, A.; Bagard, M.; Keech, O.; Gardestrom, P. The impact of light intensity on shade-induced leaf senescence.
Plant Cell Environ. 2012,35, 1084–1098. [CrossRef]
80.
Liebsch, D.; Juvany, M.; Li, Z.; Wang, H.L.; Ziolkowska, A.; Chrobok, D.; Boussardon, C.; Wen, X.; Law, S.R.; Janeckova, H.; et al.
Metabolic control of arginine and ornithine levels paces the progression of leaf senescence. Plant Physiol.
2022
,189, 1943–1960.
[CrossRef]
81.
Wu, H.Y.; Liu, L.A.; Shi, L.; Zhang, W.F.; Jiang, C.D. Photosynthetic acclimation during low-light-induced leaf senescence in
post-anthesis maize plants. Photosynth. Res. 2021,150, 313–326. [CrossRef]
82.
Guo, Y.; Gan, S.S. Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-
promoting hormonal, pathological and environmental stress treatments. Plant Cell Environ. 2012,35, 644–655. [CrossRef]
83.
Buchanan-Wollaston, V.; Page, T.; Harrison, E.; Breeze, E.; Lim, P.O.; Nam, H.G.; Lin, J.F.; Wu, S.H.; Swidzinski, J.; Ishizaki, K.;
et al. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between
developmental and dark/starvation-induced senescence in Arabidopsis. Plant J. 2005,42, 567–585. [CrossRef] [PubMed]
Int. J. Mol. Sci. 2023,24, 11996 16 of 17
84.
van der Graaff, E.; Schwacke, R.; Schneider, A.; Desimone, M.; Flugge, U.I.; Kunze, R. Transcription analysis of arabidopsis
membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol.
2006
,141,
776–792. [CrossRef] [PubMed]
85. Lin, J.F.; Wu, S.H. Molecular events in senescing Arabidopsis leaves. Plant J. 2004,39, 612–628. [CrossRef]
86.
Khanna, R.; Shen, Y.; Marion, C.M.; Tsuchisaka, A.; Theologis, A.; Schafer, E.; Quail, P.H. The basic helix-loop-helix transcription
factor PIF5 acts on ethylene biosynthesis and phytochrome signaling by distinct mechanisms. Plant Cell
2007
,19, 3915–3929.
[CrossRef] [PubMed]
87.
Qiu, K.; Li, Z.; Yang, Z.; Chen, J.; Wu, S.; Zhu, X.; Gao, S.; Gao, J.; Ren, G.; Kuai, B.; et al. EIN3 and ORE1 Accelerate Degreening
during Ethylene-Mediated Leaf Senescence by Directly Activating Chlorophyll Catabolic Genes in Arabidopsis. PLoS Genet.
2015
,
11, e1005399. [CrossRef] [PubMed]
88.
Rauf, M.; Arif, M.; Dortay, H.; Matallana-Ramirez, L.P.; Waters, M.T.; Gil Nam, H.; Lim, P.O.; Mueller-Roeber, B.; Balazadeh,
S. ORE1 balances leaf senescence against maintenance by antagonizing G2-like-mediated transcription. EMBO Rep.
2013
,14,
382–388. [CrossRef] [PubMed]
89.
He, Y.; Fukushige, H.; Hildebrand, D.F.; Gan, S. Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant
Physiol. 2002,128, 876–884. [CrossRef]
90.
Fukao, T.; Xu, K.; Ronald, P.C.; Bailey-Serres, J. A variable cluster of ethylene response factor-like genes regulates metabolic and
developmental acclimation responses to submergence in rice. Plant Cell 2006,18, 2021–2034. [CrossRef]
91.
Lee, S.C.; Mustroph, A.; Sasidharan, R.; Vashisht, D.; Pedersen, O.; Oosumi, T.; Voesenek, L.A.; Bailey-Serres, J. Molecular
characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia. New Phytol.
2011
,190, 457–471.
[CrossRef]
92.
Vashisht, D.; Hesselink, A.; Pierik, R.; Ammerlaan, J.M.; Bailey-Serres, J.; Visser, E.J.; Pedersen, O.; van Zanten, M.; Vreugdenhil,
D.; Jamar, D.C.; et al. Natural variation of submergence tolerance among Arabidopsis thaliana accessions. New Phytol.
2011
,190,
299–310. [CrossRef] [PubMed]
93.
Gasch, P.; Fundinger, M.; Muller, J.T.; Lee, T.; Bailey-Serres, J.; Mustroph, A. Redundant ERF-VII Transcription Factors Bind to
an Evolutionarily Conserved cis-Motif to Regulate Hypoxia-Responsive Gene Expression in Arabidopsis. Plant Cell
2016
,28,
160–180. [CrossRef]
94.
Loreti, E.; Valeri, M.C.; Novi, G.; Perata, P. Gene Regulation and Survival under Hypoxia Requires Starch Availability and
Metabolism. Plant Physiol. 2018,176, 1286–1298. [CrossRef] [PubMed]
95.
Giuntoli, B.; Perata, P. Group VII Ethylene Response Factors in Arabidopsis: Regulation and Physiological Roles. Plant Physiol.
2018,176, 1143–1155. [CrossRef]
96.
Fukao, T.; Yeung, E.; Bailey-Serres, J. The submergence tolerance regulator SUB1A mediates crosstalk between submergence and
drought tolerance in rice. Plant Cell 2011,23, 412–427. [CrossRef]
97.
Fukao, T.; Yeung, E.; Bailey-Serres, J. The submergence tolerance gene SUB1A delays leaf senescence under prolonged darkness
through hormonal regulation in rice. Plant Physiol. 2012,160, 1795–1807. [CrossRef]
98.
Alpuerto, J.B.; Hussain, R.M.; Fukao, T. The key regulator of submergence tolerance, SUB1A, promotes photosynthetic and
metabolic recovery from submergence damage in rice leaves. Plant Cell Environ. 2016,39, 672–684. [CrossRef]
99. Jespersen, D.; Yu, J.; Huang, B. Metabolite responses to exogenous application of nitrogen, cytokinin, and ethylene inhibitors in
relation to heat-induced senescence in creeping bentgrass. PLoS ONE 2015,10, e0123744. [CrossRef] [PubMed]
100.
Jespersen, D.; Zhang, J.; Huang, B. Chlorophyll loss associated with heat-induced senescence in bentgrass. Plant Sci.
2016
,249,
1–12. [CrossRef]
101.
Kim, C.; Kim, S.J.; Jeong, J.; Park, E.; Oh, E.; Park, Y.I.; Lim, P.O.; Choi, G. High Ambient Temperature Accelerates Leaf Senescence
via Phytochrome-Interacting Factor 4 and 5 in Arabidopsis. Mol. Cells 2020,43, 645–661. [PubMed]
102.
He, Y.; Zhang, X.; Shi, Y.; Xu, X.; Li, L.; Wu, J.L. Premature Senescence Leaf 50 Promotes Heat Stress Tolerance in Rice
(Oryza sativa L.). Rice 2021,14, 53. [CrossRef] [PubMed]
103.
Zhang, S.; Dai, J.; Ge, Q. Responses of Autumn Phenology to Climate Change and the Correlations of Plant Hormone Regulation.
Sci. Rep. 2020,10, 9039. [CrossRef] [PubMed]
104.
Wang, H.; Gao, C.; Ge, Q. Low temperature and short daylength interact to affect the leaf senescence of two temperate tree species.
Tree Physiol. 2022,42, 2252–2265. [CrossRef]
105.
Moore, B.; Zhou, L.; Rolland, F.; Hall, Q.; Cheng, W.H.; Liu, Y.X.; Hwang, I.; Jones, T.; Sheen, J. Role of the Arabidopsis glucose
sensor HXK1 in nutrient, light, and hormonal signaling. Science 2003,300, 332–336. [CrossRef]
106.
Dai, N.; Schaffer, A.; Petreikov, M.; Shahak, Y.; Giller, Y.; Ratner, K.; Levine, A.; Granot, D. Overexpression of Arabidopsis
hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence. Plant Cell
1999
,11, 1253–1266.
[CrossRef]
107.
Wingler, A.; Purdy, S.; MacLean, J.A.; Pourtau, N. The role of sugars in integrating environmental signals during the regulation of
leaf senescence. J. Exp. Bot. 2006,57, 391–399. [CrossRef]
108.
Pourtau, N.; Jennings, R.; Pelzer, E.; Pallas, J.; Wingler, A. Effect of sugar-induced senescence on gene expression and implications
for the regulation of senescence in Arabidopsis. Planta 2006,224, 556–568. [CrossRef]
109. Kim, J. Sugar metabolism as input signals and fuel for leaf senescence. Genes Genom. 2019,41, 737–746. [CrossRef]
Int. J. Mol. Sci. 2023,24, 11996 17 of 17
110. Zhang, J.; Fei, L.; Dong, Q.; Zuo, S.; Li, Y.; Wang, Z. Cadmium binding during leaf senescence in Festuca arundinacea: Promotion
phytoextraction efficiency by harvesting dead leaves. Chemosphere 2022,289, 133253. [CrossRef]
111.
Piacentini, D.; Corpas, F.J.; D’Angeli, S.; Altamura, M.M.; Falasca, G. Cadmium and arsenic-induced-stress differentially
modulates Arabidopsis root architecture, peroxisome distribution, enzymatic activities and their nitric oxide content. Plant
Physiol. Biochem. 2020,148, 312–323. [CrossRef] [PubMed]
112.
Fei, L.; Zuo, S.; Zhang, J.; Wang, Z. Phytoextraction by harvesting dead leaves: Cadmium accumulation associated with the leaf
senescence in Festuca arundinacea Schreb. Environ. Sci. Pollut. Res. Int. 2022,29, 79214–79223. [CrossRef]
113.
Sykorova, B.; Kuresova, G.; Daskalova, S.; Trckova, M.; Hoyerova, K.; Raimanova, I.; Motyka, V.; Travnickova, A.; Elliott, M.C.;
Kaminek, M. Senescence-induced ectopic expression of the A. tumefaciens ipt gene in wheat delays leaf senescence, increases
cytokinin content, nitrate influx, and nitrate reductase activity, but does not affect grain yield. J. Exp. Bot.
2008
,59, 377–387.
[CrossRef] [PubMed]
114.
Calderini, O.; Bovone, T.; Scotti, C.; Pupilli, F.; Piano, E.; Arcioni, S. Delay of leaf senescence in Medicago sativa transformed with
the ipt gene controlled by the senescence-specific promoter SAG12. Plant Cell Rep. 2007,26, 611–615. [CrossRef] [PubMed]
115.
McCabe, M.S.; Garratt, L.C.; Schepers, F.; Jordi, W.J.; Stoopen, G.M.; Davelaar, E.; van Rhijn, J.H.; Power, J.B.; Davey, M.R.
Effects of P(SAG12)-IPT gene expression on development and senescence in transgenic lettuce. Plant Physiol.
2001
,127, 505–516.
[CrossRef]
116.
Xu, Y.; Burgess, P.; Zhang, X.; Huang, B. Enhancing cytokinin synthesis by overexpressing ipt alleviated drought inhibition of
root growth through activating ROS-scavenging systems in Agrostis stolonifera.J. Exp. Bot. 2016,67, 1979–1992. [CrossRef]
117.
Cowan, A.K.; Freeman, M.; Bjorkman, P.O.; Nicander, B.; Sitbon, F.; Tillberg, E. Effects of senescence-induced alteration in
cytokinin metabolism on source-sink relationships and ontogenic and stress-induced transitions in tobacco. Planta
2005
,221,
801–814. [CrossRef]
118.
Kant, S.; Burch, D.; Badenhorst, P.; Palanisamy, R.; Mason, J.; Spangenberg, G. Regulated expression of a cytokinin biosynthe-
sis gene IPT delays leaf senescence and improves yield under rainfed and irrigated conditions in canola (Brassica napus L.).
PLoS ONE 2015,10, e0116349. [CrossRef]
119.
Khodakovskaya, M.; Li, Y.; Li, J.; Vankova, R.; Malbeck, J.; McAvoy, R. Effects of cor15a-IPT gene expression on leaf senescence in
transgenic Petunia x hybrida and Dendranthema x grandiflorum. J. Exp. Bot. 2005,56, 1165–1175. [CrossRef]
120.
Wang, H.L.; Yang, Q.; Tan, S.; Wang, T.; Zhang, Y.; Yang, Y.; Yin, W.; Xia, X.; Guo, H.; Li, Z. Regulation of cytokinin biosynthesis
using PtRD26(pro) -IPT module improves drought tolerance through PtARR10-PtYUC4/5-mediated reactive oxygen species
removal in Populus. J. Integr. Plant Biol. 2022,64, 771–786. [CrossRef]
121. Ori, N.; Juarez, M.T.; Jackson, D.; Yamaguchi, J.; Banowetz, G.M.; Hake, S. Leaf senescence is delayed in tobacco plants expressing
the maize homeobox gene knotted1 under the control of a senescence-activated promoter. Plant Cell
1999
,11, 1073–1080. [CrossRef]
122.
Guo, Y.; Gan, S. AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J.
2006
,46, 601–612.
[CrossRef] [PubMed]
123.
Liang, C.; Wang, Y.; Zhu, Y.; Tang, J.; Hu, B.; Liu, L.; Ou, S.; Wu, H.; Sun, X.; Chu, J.; et al. OsNAP connects abscisic acid and leaf
senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proc. Natl. Acad.
Sci. USA 2014,111, 10013–10018. [CrossRef]
124.
Shin, D.; Lee, S.; Kim, T.H.; Lee, J.H.; Park, J.; Lee, J.; Lee, J.Y.; Cho, L.H.; Choi, J.Y.; Lee, W.; et al. Natural variations at the
Stay-Green gene promoter control lifespan and yield in rice cultivars. Nat. Commun. 2020,11, 2819. [CrossRef] [PubMed]
125.
Kim, J.; Woo, H.R.; Nam, H.G. Toward Systems Understanding of Leaf Senescence: An Integrated Multi-Omics Perspective on
Leaf Senescence Research. Mol. Plant 2016,9, 813–825. [CrossRef] [PubMed]
126.
Woo, H.R.; Kim, H.J.; Nam, H.G.; Lim, P.O. Plant leaf senescence and death-regulation by multiple layers of control and
implications for aging in general. J. Cell. Sci. 2013,126 Pt 21, 4823–4833. [CrossRef]
127.
Zhang, Y.M.; Guo, P.; Xia, X.; Guo, H.; Li, Z. Multiple Layers of Regulation on Leaf Senescence: New Advances and Perspectives.
Front. Plant Sci. 2021,12, 788996. [CrossRef]
128.
Tseng, Y.C.; Chu, S.W. High spatio-temporal-resolution detection of chlorophyll fluorescence dynamics from a single chloroplast
with confocal imaging fluorometer. Plant Methods 2017,13, 43. [CrossRef]
129.
Iwai, M.; Yokono, M.; Kurokawa, K.; Ichihara, A.; Nakano, A. Live-cell visualization of excitation energy dynamics in chloroplast
thylakoid structures. Sci. Rep. 2016,6, 29940. [CrossRef]
130.
Zhang, Y.; Tan, S.; Gao, Y.; Kan, C.; Wang, H.L.; Yang, Q.; Xia, X.; Ishida, T.; Sawa, S.; Guo, H.; et al. CLE42 delays leaf senescence
by antagonizing ethylene pathway in Arabidopsis. New Phytol. 2022,235, 550–562. [CrossRef]
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... Abiotic stresses accelerate leaf senescence, thus resulting in reduced photosynthetic efficiency, crop yield and quality (Tan et al., 2023). CKs have long been known to inhibit leaf senescence (Richmond and Lang, 1957;Gan and Amasino, 1995) in model and crop species (Ori et al., 1999;McCabe et al., 2001). ...
... Senescent cells are characterized by increased ROS production and chlorophyll (Chl) degradation rate. ROS can cause DNA damage and activate Senescence-Associated Genes (SAGs) (Tan et al., 2023), while chlorophyll degradation allows plants to remobilize nitrogen (Khanna-Chopra, 2012). ...
... The balance between the induction of leaf senescence and the maintenance of photosynthesis can play a major role in drought tolerance and in preserving crop yields during stress in both monocot and dicot crop species (Kamal et al., 2019;Baldoni et al., 2021;Tan et al., 2023). In cereals, the stay-green response (SGR) is a secondary trait that enables crop plants to maintain their green leaves and photosynthesis capacity for a longer time after anthesis, especially under drought and heat stress conditions. ...
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Climate change-induced environmental stress significantly affects crop yield and quality. In response to environmental stressors, plants use defence mechanisms and growth suppression, creating a resource trade-off between the stress response and development. Although stress-responsive genes have been widely engineered to enhance crop stress tolerance, there is still limited understanding of the interplay between stress signalling and plant growth, a research topic that can provide promising targets for crop genetic improvement. This review focuses on Cytokinin Response Factors (CRFs) transcription factor’s role in the balance between abiotic stress adaptation and sustained growth. CRFs, known for their involvement in cytokinin signalling and abiotic stress responses, emerge as potential targets for delaying senescence and mitigating yield penalties under abiotic stress conditions. Understanding the molecular mechanisms regulated by CRFs paves the way for decoupling stress responses from growth inhibition, thus allowing the development of crops that can adapt to abiotic stress without compromising development. This review highlights the importance of unravelling CRF-mediated pathways to address the growing need for resilient crops in the face of evolving climatic conditions.
... Another alteration commonly observed in the leaves of plants exposed to TE when growing on mining sludge was the damage to chloroplast ultrastructure, such as an increase in the number and size of plastoglobuli and the distortion of the thylakoid system [26,33]. Such alterations in chloroplasts, together with nucleus condensation and the increase in cell vacuolization, are considered as stress-accelerated cell senescence [18,[83][84][85]. Accelerated cell senescence symptoms also occur as the result of water deficiency and/or high salinity stress [85]-commonly affecting plants growing on mine tailings apart from TE [2,3,5,64]. ...
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Alterations in leaf architecture can be used as an indicator of the substrate toxicity level as well as the potential of a given plant species in the phytoremediation of polluted areas, e.g., mining sludge. In this work, we demonstrated, for the first time, the nature and scale of alterations in leaf architecture at the tissue and cellular levels occurring in Norway maple growing on mining sludge originating from a copper mine in Lubin (Poland). The substrate differs from other mine wastes, e.g., calamine or serpentine soils, due to an extremely high level of arsenic (As). Alterations in leaf anatomy predominantly included the following: (1) a significant increase in upper epidermis thickness; (2) a significant decrease in palisade parenchyma width; (3) more compact leaf tissue organization; (4) the occurrence of two to three cell layers in palisade parenchyma in contrast to one in the control; (5) a significantly smaller size of cells building palisade parenchyma. At the cellular level, the alterations included mainly the occurrence of local cell wall thickenings—predominantly in the upper and lower epidermis—and the symptoms of accelerated leaf senescence. Nevertheless, many chloroplasts showed almost intact chloroplast ultrastructure. Modifications in leaf anatomy could be a symptom of alterations in morphogenesis but may also be related to plant adaptation to water deficit stress. The occurrence of local cell wall thickenings can be considered as a symptom of a defence strategy involved in the enlargement of apoplast volume for toxic elements (TE) sequestration and the alleviation of oxidative stress. Importantly, the ultrastructure of leaf cells was not markedly disturbed. The results suggested that Norway maple may have good phytoremediation potential. However, the general shape of the plant, the significantly smaller size of leaves, and accelerated senescence indicated the high toxicity of the mining sludge used in this experiment. Hence, the phytoremediation of such a substrate, specifically including use of Norway maple, should be preceded by some amendments—which are highly recommended.
... Under such conditions, photosynthetic deficiency is due to either a reduction of the content of fundamental N compounds (RuBiSCO, chlorophylls) or to an abscisic acid-dependent stomatal closure to maintain leaf water content [12,13]. In both cases, the functioning of the central metabolic pathway will be reshaped to support nutrient-recycling processes from source-to-sink leaves [14]. These processes start with the degradation of chloroplast components, producing proteins and lipids that will be rerouted toward transport processes or catabolic pathways, while mitochondria will remain metabolically active until the late stages of senescence [15][16][17]. ...
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In the context of climate change and the reduction of mineral nitrogen (N) inputs applied to the field, winter oilseed rape (WOSR) will have to cope with low-N conditions combined with water limitation periods. Since these stresses can significantly reduce seed yield and seed quality, maintaining WOSR productivity under a wide range of growth conditions represents a major goal for crop improvement. N metabolism plays a pivotal role during the metabolic acclimation to drought in Brassica species by supporting the accumulation of osmoprotective compounds and the source-to-sink remobilization of nutrients. Thus, N deficiency could have detrimental effects on the acclimation of WOSR to drought. Here, we took advantage of a previously established experiment to evaluate the metabolic acclimation of WOSR during 14 days of drought, followed by 8 days of rehydration under high- or low-N fertilization regimes. For this purpose, we selected three leaf ranks exhibiting contrasted sink/source status to perform absolute quantification of plant central metabolites. Besides the well-described accumulation of proline, we observed contrasted accumulations of some “respiratory” amino acids (branched-chain amino acids, lysineand tyrosine) in response to drought under high- and low-N conditions. Drought also induced an increase in sucrose content in sink leaves combined with a decrease in source leaves. N deficiency strongly decreased the levels of major amino acids and subsequently the metabolic response to drought. The drought-rehydration sequence identified proline, phenylalanine, and tryptophan as valuable metabolic indicators of WOSR water status for sink leaves. The results were discussed with respect to the metabolic origin of sucrose and some amino acids in sink leaves and the impact of drought on source-to-sink remobilization processes depending on N nutrition status. Overall, this study identified major metabolic signatures reflecting a similar response of oilseed rape to drought under low- and high-N conditions.
... In response to this challenge, genetic engineering of leaf senescence processes has emerged as a promising avenue for enhancing plant nutritional traits and stress tolerance. [6][7][8][9] Studies on the molecular mechanisms of leaf senescence have unveiled that it is a highly orchestrated process governed by an extensive array of senescence-associated genes (SAGs). 2,3 The functional exploration of these SAGs through reverse genetics approaches and the identification of mutants exhibiting notably altered senescence phenotypes via forward genetic screening have markedly deepened our understanding of leaf senescence. ...
... Force flowering and pod maturity of mungbean under drought stress might be due to plants possibly overcoming unfavourable stress environments by flowering a few days earlier Ahmed et al. 2008). Additionally, abiotic stresses reduced the crop maturity (including mungbean) period which was predominantly accountable for the insufficient source due to leaf senescence for the sink, resulting in decreased yield (Tan et al. 2023;Sade et al. 2018). Moreover, under drought stress condition, days to flowering and days to maturity of mungbean depends most probably on the genetic makeup of the mungbean genotypes. ...
... ERD4 can be significantly induced under salt stress treatment, enhancing plant tolerance to abiotic stress and contributing to the early stages of plant adaptation to adversity [48]. ERD10 and Response to Desiccation 29A (RD29A) activate the expression of ERF34, identified as a negative regulator of salt stress-induced leaf senescence, thereby integrating salt stress signaling with the leaf senescence program [49]. Furthermore, in this study, ERD7 was found to be induced under various stress treatments such as low temperature, NaCl, and ABA. ...
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As the final stage of leaf development, leaf senescence is affected by a variety of internal and external signals including age and environmental stresses. Although significant progress has been made in elucidating the mechanisms of age-dependent leaf senescence, it is not clear how stress conditions induce a similar process. Here, we report the roles of a stress-responsive and senescence-induced gene, ERD7 (EARLY RESPONSIVE TO DEHYDRATION 7), in regulating both age-dependent and stress-induced leaf senescence in Arabidopsis. The results showed that the leaves of erd7 mutant exhibited a significant delay in both age-dependent and stress-induced senescence, while transgenic plants overexpressing the gene exhibited an obvious accelerated leaf senescence. Furthermore, based on the results of LC-MS/MS and PRM quantitative analyses, we selected two phosphorylation sites, Thr-225 and Ser-262, which have a higher abundance during senescence, and demonstrated that they play a key role in the function of ERD7 in regulating senescence. Transgenic plants overexpressing the phospho-mimetic mutant of the activation segment residues ERD7T225D and ERD7T262D exhibited a significantly early senescence, while the inactivation segment ERD7T225A and ERD7T262A displayed a delayed senescence. Moreover, we found that ERD7 regulates ROS accumulation by enhancing the expression of AtrbohD and AtrbohF, which is dependent on the critical residues, i.e., Thr-225 and Ser-262. Our findings suggest that ERD7 is a positive regulator of senescence, which might function as a crosstalk hub between age-dependent and stress-induced leaf senescence.
... Force flowering and pod maturity of mungbean under drought stress might be due to plants possibly overcoming unfavourable stress environments by flowering a few days earlier Ahmed et al. 2008). Additionally, abiotic stresses reduced the crop maturity (including mungbean) period which was predominantly accountable for the insufficient source due to leaf senescence for the sink, resulting in decreased yield (Tan et al. 2023;Sade et al. 2018). Moreover, under drought stress condition, days to flowering and days to maturity of mungbean depends most probably on the genetic makeup of the mungbean genotypes. ...
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Mungbean is a rich source of edible protein and contributes significantly adding the atmospheric N2 to the soil. During the cultivation of mungbean, drought is one of the major constraints which negatively impact on the production of mungbean. Therefore, it is important to find eco-friendly management options to overcome drought stress. The current study was undertaken to find out the yield response of mungbean to irrigation at different pheno-phases in terms of crop growth rate (CGR), leaf area index (LAI), root growth, harvest index and water use efficiency (WUE). Treatments were two mungbean genotypes, namely BMX-08010‑2 (drought stress tolerant) and BARI Mung‑1 (drought stress sensitive) and five different irrigation schedules viz., i) No irrigation (drought stress): I0; ii) Irrigation at 1st trifoliate leaf stage (20 DAS): I1; iii) Irrigation at flowering stage (35 DAS): I2; iv) Irrigation at 1st trifoliate leaf stage (20 DAS) + flowering stage (35 DAS): I3 and v) Irrigation at 1st trifoliate leaf stage (20 DAS) + flowering stage (35 DAS) + pod-filing stage (45 DAS): I4. The study was arranged in a split-plot design distributing irrigation levels to the main plots and genotypes to the sub-plots with three replications under a rain-out shelter Calculated (based on the existing soil moisture content) irrigation water was applied manually in each treatment plot up to the field capacity level. Drought stress (no irrigation) reduced the growth and yield and shortened the life cycle. The BMX-08010‑2 genotype maintains higher performance under drought stress indicated as a drought tolerance genotype. The treatments which got two or three stages of irrigation (I3 or I4) had considerably more yield than those which got only one-stage irrigation (I1 and I2). The flowering stage (I3) was the most sensitive growth stage reducing about 18% of yield compared to the I4 treatment. It is exhibited that, if irrigation sources are available, at least two irrigation at trifoliate leaf stage (I2 at 20 DAS) and flowering stages (I3 at 35 DAS) should be ensured for obtaining higher yield. The harvest index can be increased by increasing the number of irrigation stages irrespective of irrigation at any specific stage. A strong association was also found among the growth and yield traits with the seed yield of mungbean due to different irrigation scheduling. Therefore, the parameters can be used as an effective marker to identify and develop superior genotypes suited to drought-prone environments.
Article
Nitrogen (N) is a basic building block that plays an essential role in the maintenance of normal plant growth and its metabolic functions through complex regulatory networks. Such the N metabolic network comprises a series of transcription factors (TFs), with the coordinated actions of phytohormone and sugar signaling to sustain cell homeostasis. The fluctuating N concentration in plant tissues alters the sensitivity of several signaling pathways to stressful environments and regulates the senescent-associated changes in cellular structure and metabolic process. Here, we review recent advances in the interaction between N assimilation and carbon metabolism in response to N deficiency and its regulation to the nutrient remobilization from source to sink during leaf senescence. The regulatory networks of N and sugar signaling for N deficiency-induced leaf senescence is further discussed to explain the effects of N deficiency on chloroplast disassembly, reactive oxygen species (ROS) burst, asparagine metabolism, sugar transport, autophagy process, Ca2+ signaling, circadian clock response, brassinazole-resistant 1 (BZRI), and other stress cell signaling. A comprehensive understanding for the metabolic mechanism and regulatory network underlying N deficiency-induced leaf senescence may provide a theoretical guide to optimize the source-sink relationship during grain filling for the achievement of high yield by a selection of crop cultivars with the properly prolonged lifespan of functional leaves and/or by appropriate agronomic managements.
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Leaf senescence is a complex biological process regulated at multiple levels, including chromatin remodeling, transcription, post-transcription, translation, and post-translational modifications. Transcription factors (TFs) are crucial regulators of leaf senescence, with NAC and WRKY families being the most studied. This review summarizes the progress made in understanding the regulatory roles of these families in leaf senescence in Arabidopsis and various crops such as wheat, maize, sorghum, and rice. Additionally, we review the regulatory functions of other families, such as ERF, bHLH, bZIP, and MYB. Unraveling the mechanisms of leaf senescence regulated by TFs has the potential to improve crop yield and quality through molecular breeding. While significant progress has been made in leaf senescence research in recent years, our understanding of the molecular regulatory mechanisms underlying this process is still incomplete. This review also discusses the challenges and opportunities in leaf senescence research, with suggestions for possible strategies to address them.
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Leaf senescence is a vital developmental process that involves the orderly breakdown of macromolecules to transfer nutrients from mature leaves to emerging and reproductive organs. This process is essential for a plant’s overall fitness. Multiple internal and external factors, such as leaf age, plant hormones, stresses, and light environment, regulate the onset and progression of leaf senescence. When plants grow close to each other or are shaded, it results in significant alterations in light quantity and quality, such as a decrease in photosynthetically active radiation (PAR), a drop in red/far-red light ratios, and a reduction in blue light fluence rate, which triggers premature leaf senescence. Recently, studies have identified various components involved in light, phytohormone, and other signaling pathways that regulate the leaf senescence process in response to shade. This review summarizes the current knowledge on the molecular mechanisms that control leaf senescence induced by shade.
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Salinity stress is considered the most devastating abiotic stress for crop productivity. Accumulating different types of soluble proteins has evolved as a vital strategy that plays a central regulatory role in the growth and development of plants subjected to salt stress. In the last two decades, efforts have been undertaken to critically examine the genome structure and functions of the transcriptome in plants subjected to salinity stress. Although genomics and transcriptomics studies indicate physiological and biochemical alterations in plants, it do not reflect changes in the amount and type of proteins corresponding to gene expression at the transcriptome level. In addition, proteins are a more reliable determinant of salt tolerance than simple gene expression as they play major roles in shaping physiological traits in salt-tolerant phenotypes. However, little information is available on salt stress-responsive proteins and their possible modes of action in conferring salinity stress tolerance. In addition, a complete proteome profile under normal or stress conditions has not been established yet for any model plant species. Similarly, a complete set of low abundant and key stress regulatory proteins in plants has not been identified. Furthermore, insufficient information on post-translational modifications in salt stress regulatory proteins is available. Therefore, in recent past, studies focused on exploring changes in protein expression under salt stress, which will complement genomic, transcriptomic, and physiological studies in understanding mechanism of salt tolerance in plants. This review focused on recent studies on proteome profiling in plants subjected to salinity stress, and provide synthesis of updated literature about how salinity regulates various salt stress proteins involved in the plant salt tolerance mechanism. This review also highlights the recent reports on regulation of salt stress proteins using transgenic approaches with enhanced salt stress tolerance in crops.
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NAC (no apical meristem (NAM), Arabidopsis thaliana transcription activation factor (ATAF1/2) and cup shaped cotyledon (CUC2)) transcription factors play crucial roles in plant development and stress responses. Nevertheless, to date, only a few reports regarding stress-related NAC genes are available in Malus baccata (L.) Borkh. In this study, the transcription factor MbNAC25 in M. baccata was isolated as a member of the plant-specific NAC family that regulates stress responses. Expression of MbNAC25 was induced by abiotic stresses such as drought, cold, high salinity and heat. The ORF of MbNAC25 is 1122 bp, encodes 373 amino acids and subcellular localization showed that MbNAC25 protein was localized in the nucleus. In addition, MbNAC25 was highly expressed in new leaves and stems using real-time PCR. To analyze the function of MbNAC25 in plants, we generated transgenic Arabidopsis plants that overexpressed MbNAC25. Under low-temperature stress (4 • C) and high-salt stress (200 mM NaCl), plants overexpressing MbNAC25 enhanced tolerance against cold and drought salinity conferring a higher survival rate than that of wild-type (WT). Correspondingly, the chlorophyll content, proline content, the activities of antioxidant enzymes superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT) were significantly increased, while malondialdehyde (MDA) content was lower. These results indicated that the overexpression of MbNAC25 in Arabidopsis plants improved the tolerance to cold and salinity stress via enhanced scavenging capability of reactive oxygen species (ROS).
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Senescence enables the remobilisation of nitrogen and micronutrients from vegetative tissues of wheat (Triticum aestivum L.) into the grain. Understanding the molecular players in this process will enable the breeding of wheat lines with tailored grain nutrient content. The NAC transcription factor NAM-B1 is associated with earlier senescence and higher levels of grain protein, iron, and zinc content due to increased nutrient remobilisation. To investigate how related NAM genes control nitrogen remobilization at the molecular level, we carried out a comparative transcriptomic study using flag leaves at seven time points (3, 7, 10, 13, 15, 19 and 26 days after anthesis) in wild type and NAM RNA interference (RNAi) lines with reduced NAM gene expression. Approximately 2.5 times more genes were differentially expressed in WT than NAM RNAi during this early senescence time course (6,508 vs 2,605 genes). In both genotypes, differentially expressed genes were enriched for GO terms related to photosynthesis, hormones, amino acid transport and nitrogen metabolism. However, nitrogen metabolism genes including glutamine synthetase (GS1 and GS2), glutamate decarboxylase (GAD), glutamate dehydrogenase (GDH) and asparagine synthetase (ASN1) showed stronger or earlier differential expression in WT than in NAM RNAi plants, consistent with higher nitrogen remobilisation. The use of time course data identified the dynamics of NAM-regulated and NAM-independent gene expression changes during senescence, and provides an entry point to functionally characterise the pathways regulating senescence and nutrient remobilisation in wheat.
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Complex biological processes such as plant growth and development are often under the control of transcription factors that regulate the expression of large sets of genes and activate subordinate transcription factors in a cascade-like fashion. Here, by screening candidate photosynthesis-related transcription factors in rice, we identified a DREB (Dehydration Responsive Element Binding) family member, OsDREB1C, in which expression is induced by both light and low nitrogen status. We show that OsDREB1C drives functionally diverse transcriptional programs determining photosynthetic capacity, nitrogen utilization, and flowering time. Field trials with OsDREB1C -overexpressing rice revealed yield increases of 41.3 to 68.3% and, in addition, shortened growth duration, improved nitrogen use efficiency, and promoted efficient resource allocation, thus providing a strategy toward achieving much-needed increases in agricultural productivity.
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Temperature and photoperiod are two major environmental cues shaping the leaf senescence of temperate tree species. However, how the control of leaf senescence is split between photoperiod and temperature is unknown for many ecologically important species. Here, we conducted a growth chamber experiment to test the effects of temperature (6, 9, 18, and 21°C) and photoperiod (8 and 16h daylength) on leaf senescence of two temperate tree species (Quercus mongolica and Larix principis-rupprechtii) distributed in montane forest of China. The results showed that low temperature (LT) alone could induce leaf senescence of both species under long daylength (LD) conditions, but the leaf senescence of L. principis-rupprechtii was more sensitive to the decrease in temperature than that of Q. mongolica under the LD condition. Short daylength (SD) alone could only induce the leaf senescence of L. principis-rupprechtii, suggesting that the photoperiod sensitivity varies between species. SD could accelerate the LT-induced senescence, but the effect of SD reduced with the decrease in temperature. Based on these findings, we developed a new autumn phenology model by incorporating interspecific differences in the photoperiod sensitivity of leaf senescence. Compared with the three existing process-based autumn phenology models, the new model was more robust in simulating the experimental data. When employing these models to available long-term phenological data, our new model also performed best in reproducing the observed leaf senescence date of two closely related species (Quercus robur and Larix decidua). These results enhance our understanding of how LT and SD control leaf senescence. The prediction of the climate change impacts on forest carbon uptake could be improved by incorporating this new autumn phenological model into the terrestrial biosphere models.
Article
Receptor-like kinases (RLKs) are the most important class of cell surface receptors and play crucial roles in plant development and stress responses. However, few studies were reported about the biofunctions of RLK in leaf senescence. In the current study, we characterized a novel RLK-encoding gene senescence-related receptor kinase 1 (SENRK1), which was significantly down-regulated during leaf senescence. Notably, the loss-of-function senrk1 mutants displayed an early leaf senescence phenotype, while overexpression of SENRK1 significantly delayed leaf senescence, indicating that SENRK1 negatively regulates age-dependent leaf senescence in Arabidopsis. Furthermore, the senescence-promoting transcription factor WRKY53 is able to repress the expression of SENRK1. While the wrky53 mutant showed a delayed senescence phenotype as reported, the wrky53 senrk1-1 double mutant exhibited precocious leaf senescence, suggesting that SENRK1 functions downstream of WRKY53 in regulating age-dependent leaf senescence in Arabidopsis.
Article
Nitrogen (N) deficiency causes early leaf senescence, resulting in accelerated whole-plant maturation and severely reduced crop yield. However, the molecular mechanisms underlying N deficiency-induced early leaf senescence remain unclear, even in the model species Arabidopsis thaliana. In this study, we identified Growth, Development and Splicing 1 (GDS1), a previously reported transcription factor, as a new regulator of nitrate (NO3-) signaling by a yeast-one-hybrid screen using a NO3- enhancer fragment from the promoter of NRT2.1. We showed that GDS1 promotes NO3- signaling, absorption and assimilation by affecting the expression of multiple NO3- regulatory genes including Nitrate Regulatory Gene2 (NRG2). Interestingly, we observed that gds1 mutants show early leaf senescence and reduced NO3- content and N uptake activity under N-deficient conditions. Further analyses indicated that GDS1 binds to the promoters of several senescence-related genes including Phytochrome-Interacting Transcription Factors 4 and 5 (PIF4 and PIF5) and represses their expression. Furthermore, we found that N deficiency decreases GDS1 protein accumulation and GDS1 could interact with Anaphase Promoting Complex subunit 10 (APC10). Genetic and biochemical experiments demonstrated that Anaphase Promoting Complex or Cyclosome (APC/C) complex promotes the ubiquitination and degradation of GDS1 under N deficiency, resulting in the release of PIF4 and PIF5 and consequent early senescence. In addition, we discovered that overexpression of GDS1 could delay leaf senescence and improve seed yield and N use efficiency (NUE) in Arabidopsis. Taken together, our study uncovers a molecular framework illustrating a new mechanism underlying low N-induced early leaf senescence and provides potential targets for genetic improvement of crop varieties with increased yield and NUE.