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Towards understanding abscisic acid-mediated leaf senescence

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Chengzhen Liang at Chinese Academy of Agricultural Sciences
Chengzhen Liang
Chengcai Chu at South China Agricultural University
Chengcai Chu
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*Corresponding author (email: ccchu@genetics.ac.cn)
• INSIGHT • May 2015 Vol.58 No.5: 506–508
doi: 10.1007/s11427-015-4846-z
Towards understanding abscisic acid-mediated leaf senescence
LIANG Chengzhen & CHU Chengcai*
State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental
Biology, Chinese Academy of Sciences, Beijing 100101, China
Received January 28, 2015; accepted March 13, 2015; published online April 7, 2015
Citation: Liang C, Chu C. Towards understanding abscisic acid-mediated leaf senescence. Sci China Life Sci, 2015, 58: 506–508, doi:
10.1007/s11427-015-4846-z
Senescence is a necessary part of most complex organisms
that controlled by many complicated genetic programs.
However, unlike animals and humans, leaf senescence has a
great impact on nutrient recycling from source to sink to
promote reproductive success, thus has strong adaptive ad-
vantages in plants [1,2]. Therefore, from the agricultural
point of view, understanding the process of leaf senescence
is extremely important for the breeding of higher-yielding
crop with optimized nutritional qualities.
Onset and progression of leaf senescence is controlled
primarily by developmental age, and it is also influenced by
a number of endogenous and external factors that are inte-
grated into the developmental age. Abscisic acid (ABA), a
plant hormone identified in the 1960s [3], has been regarded
as an important regulator in promoting leaf senescence.
During leaf senescence, a dramatic increase in endogenous
ABA levels is found in many plants, concomitantly with
upregulation of a subset of ABA signaling genes and se-
nescence-associated genes (SAGs), and exogenously ap-
plied ABA also induces expression of several SAGs which
accelerate leaf senescence. In addition, a variety of biotic
and abiotic stresses also elevate the ABA level and activate
signaling pathways leading to senescence. These indicate
that ABA plays a key role in regulating initiation and pro-
gression of leaf senescence; however, molecular basis of
ABA-mediated leaf senescence signaling pathway is still
largely unknown. Very recently, several components in two
model plant species Arabidopsis and rice were identified,
providing mechanistic insights into ABA-mediated leaf se-
nescence signaling [2,46].
Receptor protein kinase 1 (RPK1) is an age-dependent
action of an ABA-inducible receptor kinase, and acts as a
positive regulator of leaf senescence in Arabidopsis [4].
RPK1 encodes a membrane-bound protein that contains a
leucine-rich repeat domain at its N-terminus. Conditional
overexpression of RPK1 at the mature stage significantly
promoted leaf senescence, whereas RPK1 knockout mutant
exhibited reduced sensitivity to ABA-induced senescence.
Consistently, RPK1 is an upstream component of ABA sig-
naling and its expression is increased in an ABA-dependent
manner throughout the progression of leaf senescence.
However, induction of RPK1 expression in young plants
leads to retarded growth but does not trigger the senescence
symptoms, suggesting that function of RPK1 in ABA-
induced leaf senescence is dependent on the developmental
age.
Senescence-associated gene113 (SAG113) is a negative
regulator of ABA signaling controlling water loss during
senescence in Arabidopsis [5]. SAG113 encodes a Gol-
gi-localized PP2C family protein phosphatase, which is able
to complement the yeast PP2C-deficient ptd1 mutant, con-
firming that SAG113 is the functional ortholog of PTC1.
SAG113 is induced by ABA in senescing leaves and its ex-
pression is significantly repressed in both ABA biosynthesis
and signaling mutant aba2-1 and abi4-1. The loss-of-
function mutants of SAG113 display a delay in leaf senes-
Liang C, et al. Sci China Life Sci May (2015) Vol.58 No.5 507
cence, the stomata movement is also more sensitive to ABA,
and the water loss rate is significantly reduced. In contrast,
inducible overexpression of SAG113 causes a precocious
leaf senescence symptom, less sensitive to ABA treatment
in stomata movement, and faster water loss. These suggest
that SAG113 positively regulates ABA-induced leaf senes-
cence via inhibition of stomata closure, finally accelerates
water loss in senescing leaves.
NAP (NAC-like, activated by apetala3/pistillata) was
reported as an important positive regulator that controls leaf
senescence in both Arabidopsis and rice by four independ-
ent groups [2,68]. It encodes plant specific NAC (NAM,
ATAF1/2, CUC2) transcription activator. Overexpression of
either AtNAP or OsNAP could trigger precocious age-
dependent and dark-induced leaf senescence, and knock-
down of it significantly delayed the senescence both in Ara-
bidopsis and rice. Interestingly, AtNAP and OsNAP are spe-
cifically induced by exogenous ABA, whereas OsNAP ex-
pression is repressed in both aba1 and aba2, two ABA bio-
synthetic mutants, thus implying a possible functional simi-
larity between AtNAP and OsNAP as positive mediators of
ABA-signaling and leaf-senescence processes in plants.
Although both AtNAP and OsNAP positively regulate
ABA-mediated leaf senescence, it shows different mecha-
nisms in these two species. In Arabidopsis, AtNAP regu-
lates leaf senescence processes via directly binding to a
9-bp core sequence (CACGTAAGT) of the SAG113 pro-
moter to form an ABA-AtNAP-SAG113 PP2C regulatory
chain for controlling dehydration in senescing leaves [9].
However, in rice, OsNAP fine-tunes the leaf senescence by
directly regulating the expression of SAGs including chlo-
rophyll degradation-related genes and nutrient transport-
related genes in an age-dependent manner [2]. This differ-
ence implied that AtNAP and OsNAP may have distinctive
substrate specificities in Arabidopsis and rice. Intriguingly,
in rice, high OsNAP expression levels could repress ABA
biosynthesis via a feedback mechanism in developmental
senescence process [2]; however, which knockout of AtNAP
in Arabidopsis results in a dramatic decrease in ABA con-
tent through binding to the promoter of abscisic aldehyde
oxidase3 (AAO3, encoding the enzyme of catalyzing the last
step of ABA biosynthesis) and transactivates its expression
during dark-induced senescence [6]. This discrepancy be-
tween rice and Arabidopsis may be attributed to different
mechanisms of NAP in regulating developmental senes-
cence in rice and dark-induced senescence in Arabidopsis.
Comparative transcriptome analysis revealed that there do
exist the differences in gene expression and hormone sig-
naling pathways between developmental senescence process
and dark-induced leaf senescence [10]. To this end, a de-
tailed analysis of ABA content alterations in dark-induced
senescence of AtNAP overexpression lines as well as in de-
velopmental senescence process of atnap mutant and
AtNAP overexpression lines is imperative. Alternatively,
this discrepancy also might be due to the different species
between dicots and monocots. Nevertheless, given that
AtNAP/OsNAP is a functional ABA-mediated senescence
signaling component, these studies highlight that NAP
serves as an important link between ABA and leaf senes-
cence in higher plants.
Despite the significant progress recently in elucidating
molecular mechanism of ABA-mediated leaf senescence, it
is still at the beginning towards a full understanding of the
molecular networks of this complex biological process.
Since it is difficult to identify the genes of ABA-regulated
leaf senescence by forward genetic approach because of
functional redundancy, the identification of new compo-
nents controlling ABA-induced leaf senescence needs to be
accomplished by different approaches. A number of recent
studies demonstrated that systems biology approaches, es-
pecially by combining the different omics approaches,
should facilitate the identification of new components un-
derlying ABA-mediated leaf senescence and construction of
its complete network. On the other hand, the analysis of
natural variations during evolution and selection, combined
with genome-wide association study, should be an alterna-
tive way to identify important senescence-associated loci
that are difficult to identify using genetic approaches.
ABA is also a plant stress hormone integrating various
stress signals and controlling downstream stress responses.
Leaf senescence indeed often occurs in mutants affected in
synthesis or perception of ABA under certain stress condi-
tions. So far we did not know anything about how ABA
precisely balances its role in senescence and stress signaling
during the development of plant. Our work gave a hint that
pollination might play the crucial role in the crosstalk be-
tween ABA-induced and age-dependent senescence initia-
tion [2].
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... Leaf senescence induced by drought, high salinity, and cold stresses can promote the accumulation of endogenous ABA and the expression of ABA signaling-related genes [6,15]. Furthermore, ABA plays a positive role in regulating leaf senescence of different plant species such as Arabidopsis and rice, suggesting that ABA may play a conservative role in leaf senescence and may be a hormonal trigger of stress-induced senescence [16]. Extensive studies have demonstrated that age-dependent changes in reactive oxygen species (ROS) levels are essential for the progression of leaf senescence [11]. ...
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【Objective】As a good carrier, the premature aging mutant plays an important role in exploring the genetic mechanism and mechanism of action on premature aging, as well as improving grain yield and quality of rice.【Method】 In this study, a premature senescence mutant lps1 was obtained by EMS mutagenesis, and phenotypic observation, cytological and histochemical analysis, physiological and biochemical analysis, genetic analysis, gene localization and hormone treatment were performed on wild-type and mutants.【Result】 The leaves of lps1 began to turn yellow during the three-leaf stage, and the plant height, effective tiller number, seed-setting rate, and thousand-grain weight were extremely significantly reduced in the maturing stage. Electron microscopy observation found that the surface of lps1 leaves was smooth, the numbers of silicified protrusions and chloroplasts decreased, and the lamella structure was disordered. Physiological and biochemical analysis showed that a large amount of reactive oxygen species accumulated in mutant lps1, accompanied by protein degradation, cell membrane damage and large-scale cell death. Genetic analysis showed that the progeria phenotype was controlled by a single recessive nuclear gene, which encodes an ubiquitin conjugating enzyme on chromosome 5. The subcellular localization results prove that LPS1 protein is expressed in both the cytoplasm and the nucleus. Exogenous hormone treatment demonstrated that the lps1 was more sensitive to exogenous hormone treatment, and the LPS1 mutation promoted the expression of genes related to ABA synthesis.【Conclusion】 LPS1 mutation makes the rice ABA synthesis signal pathway abnormal, which in turn triggers abnormal changes in a series of aging-related physiological indicators such as H2O2, leading to premature senescence of lps1, and ultimately resulting in a serious decrease in rice yield.
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... On a molecular level, ABA signaling is upregulated during senescence in many plant species [14]. Some studies have reported that NAP is an important positive regulator of leaf senescence in A. thaliana and O. sativa [7][8][9][10]. ...
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... In addition, plant hormones also play crucial roles in leaf senescence. For example, ethylene (Eth) [38], abscisic acid (ABA) [39], salicylic acid (SA) [40] and jasmonic acid (JA) [41] could promote leaf senescence, while gibberellin (GA), cytokinin (CKs) and auxin can inhibit leaf senescence process [42][43][44][45]. Therefore, the mechanisms of leaf senescence are very complicated and deserve to be explored. ...
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... Moreover, drought adaptation also leads to a greater tolerance towards negative leaf water potential before the synthesis of abscisic acid is promoted (Schopfer & Brennicke 2006). Abscisic acid is known to play an important, yet complex role in leaf senescence (Liang & Chu 2015). It is therefore conceivable that the storability of broccoli was mediated by different levels of abscisic acid, which resulted from predetermination through different levels of water supply. ...
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Article
  • Sep 2018
As an essential process in the life of a plant, natural leaf senescence is necessary for adaptation to environmental diversity, whereas early leaf senescence can reduce per-unit yield and cause inferior harvest quality during crop production. To explore the molecular mechanism of leaf senescence in rice (Oryza sativa L.), we studied an early senescence leaf (esl11) mutant obtained by ethyl methane sulfonate (EMS) mutagenesis. The leaves of the esl11 mutant showed normal growth and leaf coloration prior to the three-leaf stage, but after this stage, all fully expanded leaves underwent yellowing and senescence from the edges of the leaf blade and tips, apart from the emerging leaves, which showed gradual growth. The net photosynthetic rate and photosynthetic pigment content of the tip and leaf base of the mutant esl11 were significantly lower than those of the wild type. The role of active oxygen species O2⁻, H2O2, and ×OH in the mutant increased, whereas the activities of MDA, peroxidase, superoxide dismutase, and catalase decreased compared with the wild type. The results of trypan blue staining on the senescent part of the leaf tip of the mutant esl11 indicated procedural death in part of the cell, whereas the wild type showed no change. The early leaf senescence trait in the mutant was controlled by of recessive nuclear gene, which was mapped to chromosome 7, with a physical range of 143.0 kb. The results of this study provide the foundation for important progress in gene cloning and functional analysis of the esl11 gene. © Crop Science Society of America | 5585 Guilford Rd., Madison, WI 53711 USA All rights reserved.
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A NAP-AAO3 Regulatory Module Promotes Chlorophyll Degradation via ABA Biosynthesis in Arabidopsis Leaves
Article
Full-text available
  • Dec 2014
Chlorophyll degradation is an important part of leaf senescence, but the underlying regulatory mechanisms are largely unknown. Excised leaves of an Arabidopsis thaliana NAC-LIKE, ACTIVATED BY AP3/PI (NAP) transcription factor mutant (nap) exhibited lower transcript levels of known chlorophyll degradation genes, STAY-GREEN1 (SGR1), NON-YELLOW COLORING1 (NYC1), PHEOPHYTINASE (PPH), and PHEIDE a OXYGENASE (PaO), and higher chlorophyll retention than the wild type during dark-induced senescence. Transcriptome coexpression analysis revealed that abscisic acid (ABA) metabolism/signaling genes were disproportionately represented among those positively correlated with NAP expression. ABA levels were abnormally low in nap leaves during extended darkness. The ABA biosynthetic genes 9-CIS-EPOXYCAROTENOID DIOXYGENASE2, ABA DEFICIENT3, and ABSCISIC ALDEHYDE OXIDASE3 (AAO3) exhibited abnormally low transcript levels in dark-treated nap leaves. NAP transactivated the promoter of AAO3 in mesophyll cell protoplasts, and electrophoretic mobility shift assays showed that NAP can bind directly to a segment (-196 to -162 relative to the ATG start codon) of the AAO3 promoter. Exogenous application of ABA increased the transcript levels of SGR1, NYC1, PPH, and PaO and suppressed the stay-green phenotype of nap leaves during extended darkness. Overexpression of AAO3 in nap leaves also suppressed the stay-green phenotype under extended darkness. Collectively, the results show that NAP promotes chlorophyll degradation by enhancing transcription of AAO3, which leads to increased levels of the senescence-inducing hormone ABA. © 2014 American Society of Plant Biologists. All rights reserved.
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OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice
Article
Full-text available
  • Jun 2014
Significance Premature leaf senescence is known to decrease rice yield severely, but the molecular mechanism underlying this relationship remains largely unknown. Similarly, although abscisic acid (ABA)-induced leaf senescence has long been observed, the mechanism of this pathway has yet to be determined. In this study we identified and characterized a dominant premature leaf senescence mutant, prematurely senile 1 ( ps1-D ). The data demonstrated both that PS1/Oryza sativa NAC (no apical meristem, Arabidopsis ATAF1/2, and cup-shaped cotyledon2)-like, activated by apetala3/pistillata ( OsNAP ) is an ideal marker of natural senescence onset and that it functions as an important link between ABA and leaf senescence in rice. Furthermore, reduced OsNAP expression led to extended grain filling and an improved seed-setting rate, which significantly enhanced the grain yield. Thus, fine-tuning OsNAP expression should be a means of improving rice yield.
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Identification and functional characterization of a rice NAC gene involved in the regulation of leaf senescence
Article
Full-text available
  • Sep 2013
  • BMC PLANT BIOL
As the final stage of leaf development, leaf senescence may cause the decline of photosynthesis and gradual reduction of carbon assimilation, which makes it a possible limiting factor for crop yield. NACs are plant-specific transcription factors and some NACs have been confirmed to play important roles in regulating leaf senescence. In this study, we reported a member of the NAC transcription factor family named OsNAP whose expression is associated with leaf senescence, and investigated its preliminary function during the process of leaf senescence. The results of qRT-PCR showed that the OsNAP transcripts were accumulated gradually in response to leaf senescence and treatment with methyl jasmonic acid (MeJA). A subcellular localization assay indicated that OsNAP is a nuclear-localized protein. Yeast one-hybrid experiments indicated that OsNAP can bind the NAC recognition site (NACRS)-like sequence. OsNAP-overexpressing transgenic plants displayed an accelerated leaf senescence phenotype at the grain-filling stage, which might be caused by the elevated JA levels and the increased expression of the JA biosynthesis-related genes LOX2 and AOC1, and showed enhanced tolerance ability to MeJA treatment at the seedling stage. Nevertheless, the leaf senescence process was delayed in OsNAP RNAi transgenic plants with a dramatic drop in JA levels and with decreased expression levels of the JA biosynthesis-related genes AOS2, AOC1 and OPR7. These results suggest that OsNAP acts as a positive regulator of leaf senescence and this regulation may occur via the JA pathway.
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An Abscisic Acid-AtNAP Transcription Factor-SAG113 Protein Phosphatase 2C Regulatory Chain for Controlling Dehydration in Senescing Arabidopsis Leaves
Article
Full-text available
  • Dec 2011
AtNAP is a NAC family transcription factor gene that plays a key role in leaf senescence but its underlying mechanisms are not known. SENESCENCE-ASSOCIATED GENE113 (SAG113), a gene encoding a Golgi-localized protein phosphatase 2C family protein phosphatase, mediates abscisic acid (ABA)-regulated stomatal movement and water loss specifically during leaf senescence. Here we report that SAG113 is a direct target gene of the AtNAP transcription factor. We found that both AtNAP and SAG113 were induced by leaf senescence and ABA. When AtNAP was chemically induced, SAG113 was also induced whereas when AtNAP was knocked out, the ABA- and senescence-induced expression of SAG113 was reduced. These data suggest that the expression of SAG113 is predominantly dependent on AtNAP. Functionally, overexpression of SAG113 restored the markedly delayed leaf senescence phenotype in atnap knockouts to wild type. Yeast (Saccharomyces cerevisiae) one-hybrid experiments and electrophoresis mobility shift assays showed that AtNAP could physically bind to the SAG113 promoter in vivo and in vitro, respectively. Site-directed mutagenesis revealed that AtNAP binds to a 9-bp core sequence of the SAG113 promoter, 5'CACGTAAGT3'. These results indicate that there is a unique regulatory chain, ABA-AtNAP-SAG113 protein phosphastase 2C, which controls stomatal movement and water loss during leaf senescence.
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An ABA-regulated and Golgi-localized protein phosphatase controls water loss during leaf senescence in Arabidopsis
Article
  • Feb 2012
  • PLANT J
It is known that a senescing leaf loses water faster than a non-senescing leaf and that ABA has an important role in promoting leaf senescence. However, questions such as why water loss is faster, how water loss is regulated, and how ABA functions in leaf senescence are not well understood. Here we report on the identification and functional analysis of a leaf senescence associated gene called SAG113. The RNA blot and GUS reporter analyses all show that SAG113 is expressed in senescing leaves and is induced by ABA in Arabidopsis. The SAG113 expression levels are significantly reduced in aba2 and abi4 mutants. A GFP fusion protein analysis revealed that SAG113 protein is localized in the Golgi apparatus. SAG113 encodes a protein phosphatase that belongs to the PP2C family and is able to functionally complement a yeast PP2C-deficient mutant TM126 (ptc1Δ). Leaf senescence is delayed in the SAG113 knockout mutant compared with that in the wild type, stomatal movement in the senescing leaves of SAG113 knockouts is more sensitive to ABA than that of the wild type, and the rate of water loss in senescing leaves of SAG113 knockouts is significantly reduced. In contrast, inducible over-expression of SAG113 results in a lower sensitivity of stomatal movement to ABA treatment, more rapid water loss, and precocious leaf senescence. No other aspects of growth and development, including seed germination, were observed. These findings suggest that SAG113, a negative regulator of ABA signal transduction, is specifically involved in the control of water loss during leaf senescence.
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Age-Dependent Action of an ABA-Inducible Receptor Kinase, RPK1, as a Positive Regulator of Senescence in Arabidopsis Leaves
Article
  • Mar 2011
  • PLANT CELL PHYSIOL
Leaf senescence, which constitutes the final stage of leaf development, involves programmed cell death and is intricately regulated by various internal and environmental signals that are incorporated with age-related information. ABA plays diverse and important physiological roles in plants, and is involved in various developmental events and stress responses. ABA has long been regarded as a positive regulator of leaf senescence. However, the cellular mediators of ABA-induced senescence have not been identified. We sought to understand the ABA-induced senescence signaling process in Arabidopsis by examining the function of an ABA- and age-induced gene, RPK1, which encodes a membrane-bound, leucine-rich repeat-containing receptor kinase (receptor protein kinase 1). Loss-of-function mutants in RPK1 were significantly delayed in age-dependent senescence. Furthermore, rpk1 mutants exhibited reduced sensitivity to ABA-induced senescence but little change to jasmonic acid- or ethylene-induced senescence. RPK1 thus mediates ABA-induced leaf senescence as well as age-induced leaf senescence. Conditional overexpression of RPK1 at the mature stage clearly accelerated senescence and cell death, whereas induction of RPK1 at an early developmental stage retarded growth without triggering senescence symptoms. Therefore, RPK1 plays different roles at different stages of development. Consistently, exogenously applied ABA affected leaf senescence in old leaves but not in young leaves. The results, together, showed that membrane-bound RPK1 functions in ABA-dependent leaf senescence. Furthermore, the effect of ABA and ABA-inducible RPK1 on leaf senescence is dependent on the age of the plant, which in part explains the mechanism of functional diversification of ABA action.
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Plant biology: Signal advance for abscisic acid
Article
  • Dec 2009
  • NATURE
The hunt for the receptor for abscisic acid, initially marked by false starts and lingering doubts, has met with success. Converging studies now reveal the details of how this plant hormone transmits its message.
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Comparative transcriptome analysis reveals significant differences in gene expression and signaling pathways between developmental and dark/starvation induced senescence in Arabidopsis
Article
  • Jun 2005
An analysis of changes in global gene expression patterns during developmental leaf senescence in Arabidopsis has identified more than 800 genes that show a reproducible increase in transcript abundance. This extensive change illustrates the dramatic alterations in cell metabolism that underpin the developmental transition from a photosynthetically active leaf to a senescing organ which functions as a source of mobilizable nutrients. Comparison of changes in gene expression patterns during natural leaf senescence with those identified, when senescence is artificially induced in leaves induced to senesce by darkness or during sucrose starvation-induced senescence in cell suspension cultures, has shown not only similarities but also considerable differences. The data suggest that alternative pathways for essential metabolic processes such as nitrogen mobilization are used in different senescent systems. Gene expression patterns in the senescent cell suspension cultures are more similar to those for dark-induced senescence and this may be a consequence of sugar starvation in both tissues. Gene expression analysis in senescing leaves of plant lines defective in signalling pathways involving salicylic acid (SA), jasmonic acid (JA) and ethylene has shown that these three pathways are all required for expression of many genes during developmental senescence. The JA/ethylene pathways also appear to operate in regulating gene expression in dark-induced and cell suspension senescence whereas the SA pathway is not involved. The importance of the SA pathway in the senescence process is illustrated by the discovery that developmental leaf senescence, but not dark-induced senescence, is delayed in plants defective in the SA pathway.
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AtNAP, a NAC family transcription factor, has an important role in leaf senescence
Article
  • Jun 2006
Leaf senescence is a unique developmental process that is characterized by massive programmed cell death and nutrient recycling. The underlying molecular regulatory mechanisms are not well understood. Here we report the functional analysis of AtNAP, a gene encoding a NAC family transcription factor. Expression of this gene is closely associated with the senescence process of Arabidopsis rosette leaves. Leaf senescence in two T-DNA insertion lines of this gene is significantly delayed. The T-DNA knockout plants are otherwise normal. The mutant phenotype can be restored to wild-type by the intact AtNAP, as well as by its homologs in rice and kidney bean plants that are also upregulated during leaf senescence. Furthermore, inducible overexpression of AtNAP causes precocious senescence. These data strongly suggest that AtNAP and its homologs play an important role in leaf senescence in Arabidopsis and possibly in other plant species.
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