ArticlePDF AvailableLiterature Review

The impact of multifactorial stress combination on plants, crops, and ecosystems: How should we prepare for what comes next?

November 2023
The Plant Journal 117(6)

November 2023
117(6)

DOI:10.1111/tpj.16557

Authors:

Sara I Zandalinas

University of North Texas

María Ángeles Peláez-Vico

University of Missouri

Ranjita Sinha

University of Missouri

Lidia Soto Pascual

Universitat Jaume I

Show all 5 authorsHide

The complexity of environmental conditions encountered by plants in the field, or in nature, is gradually increasing due to anthropogenic activities that promote global warming, climate change, and increased levels of pollutants. While in the past it seemed sufficient to study how plants acclimate to one or even two different stresses affecting them simultaneously, the complex conditions developing on our planet necessitate a new approach of studying stress in plants: Acclimation to multiple stress conditions occurring concurrently or consecutively (termed, multifactorial stress combination [MFSC]). In an initial study of the plant response to MFSC, conducted with Arabidopsis thaliana seedlings subjected to an MFSC of six different abiotic stresses, it was found that with the increase in the number and complexity of different stresses simultaneously impacting a plant, plant growth and survival declined, even if the effects of each stress involved in such MFSC on the plant was minimal or insignificant. In three recent studies, conducted with different crop plants, MFSC was found to have similar effects on a commercial rice cultivar, a maize hybrid, tomato, and soybean, causing significant reductions in growth, biomass, physiological parameters, and/or yield traits. As the environmental conditions on our planet are gradually worsening, as well as becoming more complex, addressing MFSC and its effects on agriculture and ecosystems worldwide becomes a high priority. In this review, we address the effects of MFSC on plants, crops, agriculture, and different ecosystems worldwide, and highlight potential avenues to enhance the resilience of crops to MFSC.

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FOCUSED REVIEW

The impact of multifactorial stress combination on plants,

crops, and ecosystems: how should we prepare for what

comes next?

Sara I. Zandalinas

, Mar

ıa



Angeles Pel

aez-Vico

, Ranjita Sinha

, Lidia S. Pascual

and Ron Mittler

2,3,*

Department of Biology, Biochemistry and Environmental Sciences, University Jaume I, Av. de Vicent Sos Baynat, s/n,

Castell

o de la Plana 12071, Spain,

Division of Plant Sciences and Technology, College of Agriculture Food and Natural Resources and Interdisciplinary Plant

Group, University of Missouri, Columbia, Missouri 65211, USA, and

Department of Surgery, University of Missouri School of Medicine, Christopher S. Bond Life Sciences Center University of

Missouri, 1201 Rollins St, Columbia, Missouri 65201, USA

Received 29 September 2023; revised 27 October 2023; accepted 10 November 2023.

*For correspondence (e-

mail mittlerr@missouri.edu).

SUMMARY

The complexity of environmental conditions encountered by plants in the ﬁeld, or in nature, is gradually

increasing due to anthropogenic activities that promote global warming, climate change, and increased

levels of pollutants. While in the past it seemed sufﬁcient to study how plants acclimate to one or even two

different stresses affecting them simultaneously, the complex conditions developing on our planet necessi-

tate a new approach of studying stress in plants: Acclimation to multiple stress conditions occurring concur-

rently or consecutively (termed, multifactorial stress combination [MFSC]). In an initial study of the plant

response to MFSC, conducted with Arabidopsis thaliana seedlings subjected to an MFSC of six different abi-

otic stresses, it was found that with the increase in the number and complexity of different stresses simulta-

neously impacting a plant, plant growth and survival declined, even if the effects of each stress involved in

such MFSC on the plant was minimal or insigniﬁcant. In three recent studies, conducted with different crop

plants, MFSC was found to have similar effects on a commercial rice cultivar, a maize hybrid, tomato, and

soybean, causing signiﬁcant reductions in growth, biomass, physiological parameters, and/or yield traits.

As the environmental conditions on our planet are gradually worsening, as well as becoming more complex,

addressing MFSC and its effects on agriculture and ecosystems worldwide becomes a high priority. In this

review, we address the effects of MFSC on plants, crops, agriculture, and different ecosystems worldwide,

and highlight potential avenues to enhance the resilience of crops to MFSC.

Keywords: agriculture, climate change, ecosystem, global warming, multifactorial, stress combination.

INTRODUCTION

Over the past 150 years human activity has been altering

our environment introducing multiple pollutants into it and

causing changes in weather patterns, soil conditions,

and air and water quality (Liu et al., 2023; Masson-

Delmotte et al., 2021; Richardson et al., 2023). The continu-

ous and unabated process of global warming caused by

the accumulation of greenhouse gases in our atmosphere

is driving, for example, an increase in day and night tem-

peratures, as well as changes in weather patterns that

include prolonged heat waves, ﬂoods, droughts, cold

snaps, and/or other extreme weather events such as

storms and torrential rains (e.g., Anderson & Song, 2020;

Bigot et al., 2018; Lehmann & Rillig, 2014; Masson-

Delmotte et al., 2021; Mazdiyasni & AghaKouchak, 2015;

Sala et al., 2000; Zandalinas, Fritschi, et al., 2021). These

affect different areas of our planet making the ‘normal’

conditions within them signiﬁcantly more extreme, or

introducing new conditions and weather patterns that are

not ‘familiar’ to the plants and crops that grow there (e.g.,

Bailey-Serres et al., 2019; Long & Ort, 2010; Mittler &

Ó2023 Society for Experimental Biology and John Wiley & Sons Ltd. 1

The Plant Journal (2023) doi: 10.1111/tpj.16557

Blumwald, 2010; Zandalinas, Fritschi, et al., 2021). These

dynamic changes in weather conditions could subject

plants and crops to rapidly changing and extreme

(‘normal’ or ‘new’) ‘abiotic stress’ conditions, as well as

combinations of two or more stress conditions occurring

simultaneously or sequentially (Bailey-Serres et al., 2019;

Zandalinas, Fritschi, et al., 2021; Zandalinas & Mittler, 2022).

Examples of such ‘abiotic stress combination’ events

include prolonged droughts combined with heat waves, a

heat wave occurring during or following a ﬂood, and alter-

nating cycles of droughts and ﬂoods. In multiple studies to

date, it was found that in many instances the combination

of two different abiotic stresses has a signiﬁcantly higher

negative impact on plant and crop growth and yield, com-

pared to each of the different stress conditions applied

individually (e.g., Azodi et al., 2020; Balfag

on et al., 2019;

Cohen et al., 2021; Gillespie et al., 2012; Orians

et al., 2019; Rizhsky et al., 2004; Ruiz-Vera et al., 2015;

Shaar-Moshe et al., 2019; Sinha et al., 2021; Sinha, Pel

aez-

Vico, et al., 2023; Slafer & Savin, 2018; Thomey et al., 2019;

Xu et al., 2023; Zandalinas et al., 2018; Zinta et al., 2014).

Adding to the different abiotic stress conditions

described above, the different changes in weather patterns

caused by human activity promote changes in the distribu-

tion and population dynamics of different pathogens and

insects, subjecting different areas of our planet to new

and/or more extreme cycles of epidemics and outbreaks,

further affecting crop yield (Becher et al., 2013; Cohen &

Leach, 2020; De Laender, 2018; Desaint et al., 2021;

Hamann, Blevins, et al., 2021). Such epidemics/outbreaks

could be caused, for example, by increased humidity due

to ﬂoods or storms/torrential rain events that promote the

spread of different bacterial and fungal pathogens, or

the warming conditions that promote the proliferation of

certain insects that could directly consume or weaken

plants and/or transmit and cause viral outbreaks (e.g.,

Cohen & Leach, 2020; Singh et al., 2023). The changes in

weather patterns, as well as other human activities, could

also cause the introduction of different invasive species,

such as weeds or parasitic plants, that would further alter

the balance within different ecosystems and/or agricultural

ﬁelds (e.g., L

opez-Tirado & Gonzalez-And

ujar, 2023; Piwo-

warczyk & Kolanowska, 2023; Ramesh et al., 2017). These

environmental ‘biotic stress’ conditions could occur in dif-

ferent combinations with the abiotic stresses described

above inﬂicting heavy losses to agricultural production

and intensifying the risk of forest ﬁres, famine, wars,

migration, and other destabilizing events (e.g., Canadell

et al., 2021; Challinor et al., 2014; Mourtzinis et al., 2015;

Prasch & Sonnewald, 2013a,2013b; Savary & Willoc-

quet, 2020; Sharma et al., 2023; Zandalinas, Fritschi,

et al., 2021).

While the different combinations of extreme abiotic

(e.g., droughts, heat waves, ﬂoods, etc.) and/or biotic

(e.g., pathogens, insects, invasive species, etc.) conditions

described above could subject crops growing in the ﬁeld

to multiple/combined stress conditions and cause a reduc-

tion in yield, other factors introduced by human activity

into our environment could also negatively impact differ-

ent plants, trees, and crops (Jacquet et al., 2014; Pascual

et al., 2022; Zandalinas, Fritschi, et al., 2021; Zandalinas,

Sengupta, et al., 2021). These include industrial, agricul-

tural, and urban pollutants that affect soil, water, and/or air

quality (e.g., Liu et al., 2023; Sigmund et al., 2023; Yang

et al., 2022). Examples of these include the contamination

of soil and water sources by heavy metals such as cad-

mium, the contamination of air by ozone and diesel parti-

cles, and/or the contamination of water sources by

nitrogen from over fertilization, or toxic spills (Shrestha

et al., 2022; Sigmund et al., 2023; Zandalinas, Fritschi,

et al., 2021). These environmental pollutants introduce a

new source of abiotic stress to plants, as well as increase

the complexity of environmental conditions experienced

by crops/plants/trees locally and globally (C^

ot

e et al., 2016;

Liu et al., 2023; Rillig, Lehmann, et al., 2021; Rillig, Ryo,

et al., 2021; Sage, 2020).

Taken together, human activity is increasing the fre-

quency, intensity, and complexity of environmental condi-

tions on our planet potentially subjecting cops, plants, and

trees to multiple abiotic and/or biotic stress conditions,

simultaneously or sequentially (Figure 1a; Pascual et al.,

2022; Zandalinas, Fritschi, et al., 2021; Zandalinas & Mit-

tler, 2022). While in the past it seemed sufﬁcient to study

how plants acclimate to one or even two different stresses

affecting it simultaneously or sequentially, the new condi-

tions developing on our planet necessitate a new approach

to studying stress in plants: Acclimation to multiple stress

conditions occurring concurrently or consecutively (Dietz &

Vogelsang, 2023; Mittler & Blumwald, 2010; Pascual

et al., 2022; Rivero et al., 2022; Zandalinas, Fritschi, et al.,

2021). This new concept of complex environmental para-

meters/stress factors affecting plants and crops was

recently termed ‘multifactorial stress combination’ (MFSC)

and deﬁned as three or more abiotic/biotic factors affecting

a plant simultaneously or sequentially (Zandalinas, Fritschi,

et al., 2021; Zandalinas & Mittler, 2022).

In an initial study of the plant response to MFSC,

conducted with Arabidopsis thaliana seedlings subjected

to an MFSC of six different low-level abiotic stresses in an

increasing level of complexity, it was found that with the

increase in the number and complexity of different stres-

ses simultaneously impacting a plant, plant growth and

survival declined, even if the effect of each stress involved

in such MFSC on the plant was minimal or insigniﬁcant

(Zandalinas, Sengupta, et al., 2021). This ﬁnding was the

basis for formulating the plant ‘MFSC principle’ that

states that: ‘With the increasing number and complexity

of different stressors simultaneously impacting a plant

Ó2023 Society for Experimental Biology and John Wiley & Sons Ltd.,

The Plant Journal, (2023), doi: 10.1111/tpj.16557

2Sara I. Zandalinas et al.

1365313x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/tpj.16557 by Consorci De Serveis Universitaris De Catalunya, Wiley Online Library on [26/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License

(i.e., MFSC), plant growth, survival, and/or yield will

decline dramatically, even if the effects of each individual

stress involved in such MFSC on the plant is minimal or

insigniﬁcant’ (Figure 1b; Zandalinas, Fritschi, et al., 2021;

Zandalinas & Mittler, 2022). Since then, MFSC has been

shown to have a similar effect on a commercial rice culti-

var, a maize hybrid, tomato, and soybean, causing signiﬁ-

cant reductions in growth, biomass, physiological

performance, and/or yield parameters (Pascual

et al., 2023; Pel

aez-Vico et al., 2023; Sinha, Pel

aez-Vico,

et al., 2023). These ﬁndings highlight the serious threat

MFSC poses to current and future agricultural operations,

open the way to new studies into this important subject,

and underline the need for dedicated breeding and engi-

neering programs to enhance the resilience of crops to

MFSC (Rivero et al., 2022; Zandalinas & Mittler, 2022). As

the environmental conditions on our planet are gradually

worsening, as well as becoming more complex (Lehmann

& Rillig, 2014; Rillig, Lehmann, et al., 2021; Rillig, Ryo,

et al., 2021; Zandalinas, Fritschi, et al., 2021; Zandalinas &

Mittler, 2022), addressing MFSC, and its effects on agricul-

ture and ecosystems worldwide, becomes a high priority.

In this review, we will address the impacts of MFSC on

plants, molecular pathways, different ecosystems, and

agriculture, and highlight potential avenues to enhance

the resilience of crops to MFSC.

THE EFFECTS OF MFSC ON PLANTS

To begin, we will focus on the effects of MFSC/stress com-

bination on plants, plant physiology, and plant reproduc-

tion. Early studies of ‘simple’ stress combinations, such as

drought and heat, revealed that under conditions of stress

combination different physiological pathways can have

conﬂicting interactions. A classic example of this, observed

in many different plants since its initial discovery in

tobacco and Arabidopsis (Rizhsky et al., 2002,2004), is the

conﬂicting response of stomata to a drought and heat

stress combination (e.g., Sinha et al., 2022; Zandalinas,

Balfag

on, et al., 2016; Zandalinas, Fichman, et al., 2020;

Zandalinas, Rivero, et al., 2016). Thus, in response to

heat stomata are kept open to cool leaves by transpiration

(e.g., Zandalinas, Fichman, et al., 2020; Zandalinas, Rivero,

et al., 2016; Zhou et al., 2015; Figure 2a), while in response

to drought stomata close to prevent leaves from dehydra-

tion (Hsu et al., 2021; Nilson & Assmann, 2007; Sun

et al., 2014; Figure 2a). In response to a combination of

drought and heat, stomata remain close, and transpiration

is suppressed. This results in higher overall leaf tempera-

ture during a combination of drought and heat stress, com-

pared to heat alone, and could be one of the main reasons

this stress combination is affecting crop yield in such a

severe manner in the ﬁeld. Recently, the general stomatal

Number of stressors combined

MULTIFACTORIAL

STRESS COMBINATION

Biotic

Stressors

Parasitic plants

Bacteria

Grazing

Fungal

Virus

Insect

PLANT GROWTH AND

YIELD REDUCTIONS

Climatic

Stressors

Flood

Ozone

Heat or Cold

Drought

Wind

Freezing

Soil

Stressors

Nutrient deficiency

Microbiome decline

Salinity

Anthropogenic

Stressors

Burn/diesel particles

Heavy metals

Microplastics

Organic pollutants

Pesticides

Herbicides

eCO2

(a)

Soil respiration and

decomposition rate

Ecosystem services

Plant growth and

survival

Soil biodiversity

richness

% of Control

100

0123456789…

(b)

Figure 1. The impact of multifactorial stress combination on plants, crops, ecosystems, and soils.

(a) The different types of stressors that could potentially impact plants and crops in different combinations. Multifactorial stress combination occurs when three

or more stresses impact a plant or a crop simultaneously or sequentially.

(b) The multifactorial stress combination principal: With the increase in the number and complexity of different stressors simultaneously impacting a plant, crop,

ecosystem, and/or soil microbiome, their overall health and/or services will decline, even if the effects of each stress involved in such a multifactorial stress com-

bination is minimal or insigniﬁcant. Adapted from Rillig et al. (2019), Zandalinas, Sengupta, et al. (2021), and Zandalinas and Mittler (2022).

Ó2023 Society for Experimental Biology and John Wiley & Sons Ltd.,

The Plant Journal, (2023), doi: 10.1111/tpj.16557

Multifactorial stress combination 3

response of soybean to MFSC was also shown to be an

overall closure response (Pel

aez-Vico et al., 2023), while in

tomato stomatal responses to MFSC were more diverse

and depended on the context of the different stress combi-

nations involved in the MFSC (Pascual et al., 2023). While

these, and many other studies, were conducted with

leaves, new ﬁndings reveal that the stomatal response of

soybean leaves and ﬂowers (sepals) to stress combination

is different (Sinha et al., 2022). Thus, in response to a com-

bination of drought and heat stress stomata on leaves

were close, while stomata on ﬂowers (sepals) remained

open, allowing the cooling of ﬂowers, and preventing

heat-associated damages to reproductive processes (Sinha

et al., 2022). This newly discovered strategy of plant accli-

mation to stress combination was termed ‘Differential

Transpiration’ and proposed to play an important role in

protecting crop yield from different stress combinations,

especially in crops that are Cleistogemic (i.e., fertilization

occurs while ﬂowers are closed; Campbell et al., 1983),

such as soybean, wheat, and rice (Sinha et al., 2022; Sinha,

Shostak, et al., 2023). In addition to drought and heat

stress combination, differential transpiration could also

Heat Stress

Open Stomata

Close Stomata

Salinity

(a)

(c)

Heat

Light Stress

Herbicides

Water Deficit

Salinity

Nutrient

Stress

Acidity

Heat

High light

Herbicides

Water Deficit

Salinity

Nutrient

Stress

Heavy Metals

Acidity

Cumulative/Conflicting

Models

Intermediate effect

Secondary or less pronounced effect

(b)

Pathogens

Drought

Nutrient

Stress

Air pollution

Other

Stresses

Heat Stress

Light Stress

Drought Stress

Salinity Stress

Pathogens

Nutrient Stress

Soil pollutants

Cold Stress

Air pollution

All together (MFSC)

Photosynthesis

Transpiration

(stomata)

Reproduction

Hormonal balance

Growth

Nutrient uptake

Crop

survival

and

growth

Conflicting Model

Low High

Intensity of Effect

Most pronounced effect

Figure 2. Interactions between different physiological processes during multifactorial stress combination.

(a) The effects different types of stressors have on stomatal conductance, and some of the potential outcomes of combinations such as drought or salt and heat

stress.

(b) The cumulative versus conﬂicting models for the effects of different stresses on the overall physiological processes of plants during multifactorial stress

combination. ‘

Cumulative’ is depicted by the additive effect of multiple low-level stresses on the plant (many same-size circles that co-occur during multifactorial

stress combination), while ‘Conﬂicting’ is depicted by the larger effect of certain stresses involved in the multifactorial stress combination on the plant (few

larger circles that co-occur during multifactorial stress combination). Adapted and modiﬁed from Zandalinas and Mittler (2022).

(c) Speciﬁc examples for the different intensities of the conﬂicting effect between different stresses (visualized by the thickness of the different lines that connect

each combination of two different stresses) on the growth (left panel) or photosynthesis (right panel) of soybean, tomato, maize, and rice plants. Adapted from

Pascual et al. (2023), Pel

ez-Vico et al. (2023), Sinha, Pel

aez-Vico, et al. (2023) and Zandalinas and Mittler (2022). MFSC, multifactorial stress combination.

Ó2023 Society for Experimental Biology and John Wiley & Sons Ltd.,

The Plant Journal, (2023), doi: 10.1111/tpj.16557

4Sara I. Zandalinas et al.

play an important role in stress combinations that involve

heat and other stresses that cause stomatal closure, such

as ozone, high CO

, pathogen infection, high light, and

MFSC (Sinha et al., 2022; Sinha, Shostak, et al., 2023). In

future studies, it would be important to test the differential

transpiration response of plants subjected to MFSC, espe-

cially ones that display a leaf overall stomatal closure

response to MFSC, such as soybean (Pel

aez-Vico

et al., 2023). It would also be important to determine what

is the signiﬁcance of stomatal responses measured in the

greenhouse, and laboratory settings, to ﬁeld conditions

(Bernacchi et al., 2007; Jarvis & McNaughton, 1986).

In addition to stomatal responses, MFSC was shown to

have an overall negative effect on other physiological and

metabolic processes such as photosynthesis (Hamann,

Denney, et al., 2021; Pascual et al., 2023; Pel

aez-Vico

et al., 2023; Xu et al., 2023) and the accumulation of differ-

ent osmo-protectants (e.g., proline; Pascual et al., 2023;

Figure 2b). These were further associated with an overall

decrease in plant growth rate, height, biomass, and yield

(Pascual et al., 2023; Pel

aez-Vico et al., 2023). While the

cause of these reductions is unknown at present, two possi-

ble models/scenarios can explain it: (i) A ‘cumulative effect’

occurs between the same or different low-level impacts of

each different stress (that compose the MFSC) on plant

physiology, metabolism, and molecular responses, causing

an overall reduction in growth, yield, and survival. Thus,

while each different stress has a small (similar or different)

effect on plant physiology and metabolism when applied

individually, when the different stresses are combined dur-

ing MFSC, their effects are cumulative, and the more stres-

ses combined the stronger the effect will be

(Zettlemoyer, 2023; Figure 2b); and (ii) a ‘conﬂicting interac-

tion effect’ between different physiological, metabolic,

and/or molecular responses during two or more speciﬁc

stresses (that are part of the MFSC) are dominating the

impacts of MFSC and causing an overall reduction in

growth and yield, as plants are unable to balance their

metabolism and energy ﬂow through the different path-

ways that should be coordinated (Figure 2c). It is of course

highly likely that, under natural conditions, or in the ﬁeld, a

combination of the two scenarios/models outlined above

(i.e., conﬂicting versus cumulative models; Figure 2b)

occurs in plants subjected to MFSC. In addition, it may be

possible that some of the conﬂicting interactions between

two or more stresses, occurring during MFSC, could have

beneﬁcial effects on plants. For example, the closing of sto-

mata during MFSC could protect plants from ozone stress

or pathogen attack (Gupta et al., 2016; Iyer et al., 2013; Mit-

tler, 2006). While some pathways and processes may have

conﬂicting or additive ‘negative’ effects (Figure 2), other

pathways/processes co-activated during MFSC could there-

fore have an additive ‘positive’ effect and together help the

plant mitigate some of the effects of the stress combination

(for a more detailed review of potential positive and

negative interactions between different stresses/pathway-

s/processes, please see Zandalinas & Mittler, 2022). Another

aspect to consider in this respect is the distinction between

stresses that are mediated by limited resource availability

(e.g., water, nutrients, and/or light), as opposed to stresses

that are mediated by non-resources (e.g., temperature

and/or different air, water, and soil pollutants). These two

can interact, as the non-resource-driven stresses can affect

the availability of resources and cause resource-limited-

induced stresses (Cossani & Sadras, 2018; Sperfeld et al.,

2012; Weih et al., 2021). In light of these potential interac-

tions and their outcomes (i.e., ‘positive’/‘negative’ additive,

semi-additive, conﬂicting, or synergistic; Zandalinas & Mit-

tler, 2022), further studies are needed to address the multi-

ple possible interactions occurring during different MFSCs.

Due to the large differences in developmental pro-

grams, cellular differentiation patterns, overall anatomy,

and physiological, metabolic, and signaling network con-

texts, between reproductive and vegetative tissues, it is

likely that MFSC will affect these two tissues differently

(Figure 3a). These differences could result from differential

sensitivities of the various networks and pathways that dis-

tinguish between these two tissues, as well as from the

overall sensitivity of the critical processes that each tissue

is mediating (e.g., photosynthesis and energy manage-

ment in leaves, as opposed to reproduction and differentia-

tion in ﬂowers/pods) to MFSC. While vegetative tissues

might be more resilient to stress combinations that include

heat stress, reproductive tissues, for example, are likely to

be more sensitive to them (Sinha et al., 2021). It was

recently reported that a combination of salinity and acidity

stresses had the most pronounced effect on soybean

leaves, while soybean ﬂowers were primarily impacted by

drought, and drought combined with heat (Pel

aez-Vico

et al., 2023). Moreover, the overall transcriptomic response

of soybean ﬂowers to stress combination/MFSC was found

to be very different from that of leaves (Pel

aez-Vico

et al., 2023; Sinha et al., 2022; Figure 3b). The differences

between the sensitivity of vegetative and reproductive tis-

sues to MFSC, coupled with the different roles each tissue

is responsible for and its relative importance to yield and

growth of different crops (e.g., importance of leaves for

biomass and growth, in biomass crops, as opposed to

importance of ﬂowers to reproduction, in grain crops),

highlight the need to initiate and promote dedicated

research programs directed at each tissue and its response

to stress combination/MFSC. Genes, networks, and path-

ways that may be effective in enhancing the resilience of

vegetative tissues to MFSC may therefore have no, or even

negative, beneﬁcial effect(s) on the resilience of reproduc-

tive tissues to MFSC (and vice versa). Altering the function

of speciﬁc genes/pathways/networks in different tissues

will also require tissue-, and stress combination/MFSC-

Ó2023 Society for Experimental Biology and John Wiley & Sons Ltd.,

The Plant Journal, (2023), doi: 10.1111/tpj.16557

Multifactorial stress combination 5

speciﬁc promoters that need to be identiﬁed in

different crops (Sinha, Induri, et al., 2023). Taken together,

the recent studies focused on the molecular response of

vegetative and reproductive tissues to stress combina-

tion/MFSC suggest that attempting to enhance the overall

resilience of crops to climate change/stress combina-

tion/MFSC would require a coordinated approach that

simultaneously alters the expression of different groups of

transcripts in different tissues in a stress- and/or tissue-

speciﬁc manner. Such an approach will require dedicated

research and breeding programs and is discussed in more

detail below. To better understand the effects of MFSC on

plants we will next explore how this unique state of stress

combination affects different molecular pathways.

EFFECTS OF MFSC ON MOLECULAR PATHWAYS

As indicated above, the molecular responses of seedlings,

leaves, and ﬂowers of different plants to MFSC are unique.

Much like ‘simple’ stress combinations, such as drought

and heat, salt and heat, or heat and high light (Azodi

et al., 2020; Balfag

on et al., 2019; Rizhsky et al., 2002,2004;

Sinha et al., 2022; Sinha, Induri, et al., 2023; Sinha, Shos-

tak, et al., 2023; Zandalinas, Sengupta, et al., 2021), the

transcriptomic response of plants to each of the different

stresses/stress combinations that compose the MFSC was

found to be distinct. These differences were further found

to be reﬂected in the different transcription factor (TF) net-

works altered in plants in response to each stress combina-

tion/MFSC (Sinha, Induri, et al., 2023; Zandalinas, Fritschi,

et al., 2020; Zandalinas, Sengupta, et al., 2021). For exam-

ple, when the transcripts under the control of the TF heat

shock factor A2 (HSFA2) were compared between soybean

leaves subjected to heat stress, drought, or drought and

heat stress combination, it was found that although HSFA2

was induced under all of these stresses, there was almost

no overlap between the transcripts it regulated under each

of these different conditions (potentially a result of its inte-

gration into larger TF networks that were differently altered

under each of the different stress conditions) (Sinha,

Induri, et al., 2023; Figure 4). While different TFs may regu-

late the same or different programs/pathways in the cell

and their overall expression pattern, or expression land-

scape, could orchestrate or integrate the overall response

of plants to the different combinations of stresses it is sub-

jected to during MFSC, some of the pathways and pro-

grams that may be co-activated, could have a conﬂicting

effect on plant metabolism, signaling and acclimation.

Examples of these could include the co-activation of accli-

mation pathways for heat, drought, or salt in plants sub-

jected to MFSC, which may require conﬂicting regulatory

networks (Zandalinas, Fritschi, et al., 2020; Zandalinas &

Mittler, 2022). Other examples of conﬂicting metabolic and

molecular pathways, that could affect growth and repro-

duction in plants/crops during MFSC, include negative

interactions between different phytohormone signaling

pathways such as abscisic acid and salicylic acid, and/or

negative interactions between different pathways involved

in the biosynthesis and/or accumulation of different osmo-

protectants and/or antioxidants, and pathogen defense

pathways that could potentially lead to negative interac-

tions between defense and acclimation pathways during

different stresses/MFSCs (Atkinson & Urwin, 2012; Berens

et al., 2019; Kim et al., 2017; Saijo & Loo, 2020; Yasuda

et al., 2008; Zandalinas et al., 2022). The different examples

outlined above could further be viewed through the lens of

the conﬂicting versus cumulative impact models that try to

explain the overall effects of MFSC on plant growth and

reproduction (see above; Figure 2b,c). Further studies,

including more detailed exploration and dissection of dif-

ferent networks and pathways during MFSC, are of course

Differential transcriptomic responses

Decreased:

• Chlorophyll content

• Photosynthetic rate

• Leaf water status

• Biomass

• Stomatal

conductance

• Growth rate

• Nutrient balance

Decreased:

• Pollen viability,

germination and growth

• Pistil receptivity and

function

• Fertilization

• Embryogenesis

• Ovary and egg viability

• Seed filling

Differential

Physiological/

developmental

responses

Reproductive

Vegetative

(a) (b)

Biotic Stressors

Anthropogenic

Stressors

Climate

Stressors

Soil Stressors

Figure 3. Vegetative and reproductive tissues have differential responses to stress combination.

(a) Some of the differences in physiological and developmental processes impacted by stress combination/multifactorial stress combination in plants.

(b) The differential transcriptomic response of vegetative and reproductive tissues to water deﬁcit, heat stress, and their combination. Adapted from Pel

ez-Vico

et al. (2023), Sinha et al. (2022), and Sinha, Shostak, et al. (2023). HS, heat stress; WD, water deﬁcit.

Ó2023 Society for Experimental Biology and John Wiley & Sons Ltd.,

The Plant Journal, (2023), doi: 10.1111/tpj.16557

6Sara I. Zandalinas et al.

needed to address each of the different combinations of

MFSC conditions, their molecular and metabolic

responses, and the TF, hormones, and other signaling

reactions that control them, and this analysis should be fol-

lowed by studying gain- and loss-of-function mutants.

Taken together, the examples outlined above highlight

one of the major challenges plants could experience during

MFSC. While some of the stress combinations/MFSC condi-

tions that induce these conﬂicting responses in plants and

crops grown in the ﬁeld are in line with ‘normal’ conditions

(e.g., combinations of drought, salinity, heat, cold, and/or

ﬂood, that are simply becoming more extreme and/or com-

plex), some MFSC might be ‘new’ to plants (e.g., combina-

tions of human-generated air, water, and soil pollutants,

such as heavy metals, diesel particles, and different micro-

plastics, with the more ‘normal’ stresses such as drought,

heat, salt, etc.). The key difference between these two

groups of MFSC (‘new’ versus ‘normal’), is that plants might

have evolved over millions of years to adapt to the more

‘normal’ MFSCs, but they had less than 150 years to adapt

to the ‘new’ types of MFSCs. As plants and their molecular

pathways are interlinked with the environment and other

organisms within their growth habitat, we will next discuss

the potential effects of MFSC on different ecosystems.

EFFECTS OF MFSC ON ECOSYSTEMS

The past several years have seen the publication of several

new studies on the effects of MFSC on different ecosystems

worldwide (e.g., Adams et al., 2019; Anderegg et al., 2020;

Bryndum-Buchholz et al., 2019; Forzieri et al., 2021; Hubbart

et al., 2016; Kroeker et al., 2013; McDowell et al., 2020; Pasc-

ual et al., 2022; Seidl et al., 2017; Sigmund et al., 2023). In

general, it was found that multiple stressors impacting an

ecosystem cause a reduction in ecosystem (life-supporting)

services, which is often coupled with a reduction in species

diversity (Becher et al., 2013; Osburn et al., 2023; Rillig

et al., 2019,2023; Yang et al., 2022; Figure 1b). Interestingly,

species diversity appears to be less vulnerable to MFSC

than ecosystem services, potentially due to the replacement

of established species that are more sensitive to MFSC with

new species that are more resilient to it. In some extreme

cases, however, MFSC could lead to an ecosystem ‘col-

lapse’, for example when it leads to massive forest ﬁres or

large die-outs of marine species in rivers or lagoons

(Adams et al., 2019; Bryndum-Buchholz et al., 2019; Pop-

kin, 2021; Sigmund et al., 2023). These are usually slow to

rebound and could promote invasive species and other

complicating parameters that lead to the establishment of

less complex ecosystems. Some examples of such ecosys-

tems are given below (Figure 5).

Forests could undergo dramatic transformations due

to the impact of multifactorial stresses associated with cli-

mate change. The intricate vegetative dynamics, structural

complexities, and beneﬁts/services of forests to our society

are signiﬁcantly inﬂuenced by different stressors, including

temperature extremes, high CO

, and an increase in vapor

101 125

269

202

WD HS

WD+HS

213

WD+HS

HSFA2

TFs with log 2-fold < 1

TFs with log 2-fold > 1

No DE TFs

non-TFs with log 2-fold > 1

non-TFs with log 2-fold < 1

(a)

(b)

Figure 4. Differential control of transcriptional regulatory networks in soybean during stress combination.

(a) Gene regulatory network maps showing the expression pattern of different leaf transcriptional networks under the control of the heat shock factorA2

(HSFA2) during water deﬁcit (WD), heat stress (HS), and their combination (WD

+HS). Arrows next to each stress indicate the number of transcripts with a sig-

niﬁcant change (enhanced in red and suppressed in blue) in their expression (>twofold).

(b) A Venn diagram showing the overlap between the different transcripts enhanced or suppressed by HSFA2 during the different stresses. Adapted from Sinha,

Induri, et al. (2023). Stress conditions were as follows: WD, irrigated daily with only 30% of water available for transpiration; HS, 38/28°

C day/night (control was

at 28/24°C day/night). DE, differential expression; HS, heat stress; TF, transcription factor; WD, water deﬁcit.

Ó2023 Society for Experimental Biology and John Wiley & Sons Ltd.,

The Plant Journal, (2023), doi: 10.1111/tpj.16557

Multifactorial stress combination 7

pressure deﬁcit. These, contribute to heightened forest

mortality and increased susceptibility to insect outbreaks,

wildﬁres, soil erosion, and wind disturbances (McDowell

et al., 2020). For example, between 2019 and 2020, a series

of mega-ﬁres (known as the ‘Black Summer’ ﬁres) devas-

tated approximately 5.8 million hectares within the tem-

perate forest ecosystem of Australia. These destructive

ﬁres occurred concurrently with a historic period of excep-

tionally low rainfall and intense heat (Canadell et al., 2021).

In addition, extreme weather events, including prolonged

droughts, or intense precipitation, coupled with warmer

temperatures, are leading to increased tree mortality

worldwide. For example, the rapid decline in the dominant

forest species Quercus alba (white oak) in the US Midwest

has been associated with periods of excessive rainfall

under a warming climate (Hubbart et al., 2016). The

increased frequency of extreme wet weather likely contrib-

uted to the emergence of biotic stressors include fungal-

like oomycetes and other pathogens, that led to root dam-

age and ultimately tree mortality (Hubbart et al., 2016). The

impacts associated with climate change/MFSC pose a

grave risk to forests, threatening their role as carbon sinks

and biodiversity sanctuaries. These effects may alter the

distribution of tree species and forest communities, disrupt

the carbon cycle, and render forests more susceptible to

various other stressors and/or pathogens/pests (Anderegg

et al., 2020; Forzieri et al., 2021; Hamann, Denney, et al.,

2021; Seidl et al., 2017). A comprehensive analysis of cli-

mate effects on forests revealed for example that the com-

bined effects of different stressors tend to magnify carbon

losses (Anderegg et al., 2020; Seidl et al., 2017).

Aquatic ecosystems are also in danger due to the

complexity of stresses associated with climate change

(Sigmund et al., 2023). The Indian River lagoon ecosystem,

recognized as one of North America’s most biodiverse

estuaries, has for example faced numerous challenges,

including habitat alterations, incidents of toxic spills,

industrial and agricultural pollution, and the impact of

global warming on water temperature. Consequently, this

ecosystem has experienced harmful algal blooms that led

to the death of seagrass, marine life, and birds (Adams

et al., 2019). Losses in marine biodiversity have also been

associated with high greenhouse gas emissions, with a

potential for a 15–30% reduction in total marine animal

biomass by 2100 in the North and South Atlantic and

Paciﬁc, as well as in the Indian Ocean (Bryndum-Buchholz

Warming

SOIL

MICROBIOMES

RIVERS

Pests

Wind

Fire

Soil

pollutants

Drought

CO2

Flood

Toxic spills

FORESTS

Ice melting

Salinity

Microplastics

LAKES

Human

activities

LAGOONS

OCEANS

Agricultural

spills

Algal blooms

Warm in g

Figure 5. Some of the different combinations of stressors that could potentially impact different ecosystems around the world and cause multifactorial stress

combination. The major ecosystem depicted are forests, rivers, lagoons, and oceans. See text for more details.

Ó2023 Society for Experimental Biology and John Wiley & Sons Ltd.,

The Plant Journal, (2023), doi: 10.1111/tpj.16557

8Sara I. Zandalinas et al.

et al., 2019). Ocean acidiﬁcation, as a result of increased

atmospheric CO

levels (Doney et al., 2020), can also lead

to shifts in marine population dynamics and organism

physiology, altering ecosystems and communities. When

marine species are simultaneously exposed to elevated

and rising temperatures, decreased survival and

slower growth and development are observed (Kroeker

et al., 2013). The co-occurrence of multiple stress factors is

also predicted to increase the intensity, frequency, and

duration of cyanobacterial blooms in different eutrophic

reservoirs, lakes, and estuaries, producing hepatotoxins,

neurotoxins, and/or dermatoxins, that can affect mammals

and birds. For example, toxic cyanobacteria have been

found in Lake Erie (USA), Lake Taihu (China), Lake Victoria

(Africa), Lake Okeechobee (USA), and the Baltic Sea (Jans-

son & Hofmockel, 2019).

Soils are an important source of terrestrial biodiversity

providing habitats to nearly a quarter of all Earth’s species.

The soil microbiome is key for the cycling of nutrients,

contributing to plant and animal growth, and maintaining

soil health for future generations (Jansson & Hofmockel,

2019; Osburn et al., 2023). Climate change is modifying the

diversity and structure of microbial communities (Rillig

et al., 2019; Zhou et al., 2020). Signiﬁcant alterations in

bacterial and fungal biodiversity were for example found

in forest soils with an annual temperature of more than

20°C on average, as well as in response to warming across

a 9-year study of tall-grass prairie soils (Jansson & Hof-

mockel, 2019). Arbuscular mycorrhizal fungi (AMF) are key

symbiotic microorganisms for many terrestrial plants, and

AMF diversity is associated with plant productivity

and therefore ecosystem stability and sustainability (Jef-

fries et al., 2003). AMF can enhance water and nutrient

uptake in plants, as well as resistance to several abiotic

stresses such as drought (Alguacil et al., 2021). Neverthe-

less, in soils exposed to abiotic stresses such as salinity,

heavy metal pollution, drought, fungicides, and/or extreme

pH, AMF diversity decreases, impacting plant growth and

reproduction (Edlinger et al., 2022; Fu et al., 2022; Lenoir

et al., 2016). A recent study examining the effects on soils

of different combinations of up to 10 global change factors

including different abiotic factors, toxic compounds (inor-

ganic and synthetic organic), and microplastics, demon-

strated that the complexity, composition, and overall

abundance of soil microbiomes declined with the increase

in the number of factors impacting soils simultaneously

(Rillig et al., 2019; Figure 1b). In addition, it was recently

shown that the positive effect of soil microbial diversity on

soil functions and properties was reduced by the simulta-

neous occurrence of different global change factors includ-

ing salinity, warming, N deposition, heavy metal, plastic

mulching ﬁlm residues, fungicide, drought, bactericide,

surfactant contaminant, and soil compaction (Yang et al.,

2022; Figure 1b).

Taken together, the examples discussed above reveal

that, due to human intervention, almost all aspects of life

on our planet could be affected by MFSC. This possibility

is highly worrisome and should be addressed at multiple

levels, from the personal and individual levels to the gov-

ernment and society levels, and globally. We will next

address the potential impacts of MFSC on agriculture.

EFFECTS OF MFSC ON CROP PLANTS

In a sharp contrast to ecosystems, that contain multiple

and interconnected species, agricultural systems mostly

involve a single central species (the crop being cultivated,

and its supporting microbiomes/cover crops and other spe-

cies, involved in the different agricultural practices used

and acreage covered) and could therefore be highly prone

to stress combination/MFSC. The risk for agriculture is

especially critical due to the gradual increase in day/night

temperatures and the increase in the frequency and inten-

sity of extreme weather events and levels of pollutants in

recent years (Figure 6). Several different studies have

recently revealed that microbiomes, that support plant

growth, are negatively impacted by MFSC (Edlinger et al.,

2022; Rillig et al., 2019,2023; Yang et al., 2022; Figure 1b).

Anthropogenic activities are also altering soil biological,

chemical, and physical properties (e.g., Rillig et al., 2019;

Yang et al., 2022), as well as causing a slow increase in the

levels of soil, water, and air contaminants (Liu et al., 2023;

Masson-Delmotte et al., 2021; Richardson et al., 2023) that

could affect crops, especially ones grown near industrial

and/or highly populated zones, for example, in Europe. In

addition to generating pollution, the expansion of societies

and cities is also causing a decrease in the availability of

prime agricultural land for the cultivation of crops (Borrelli

et al., 2020; Grimm et al., 2008). In some countries there-

fore crop cultivation is ‘pushed’ into areas that are not

ideal for plant growth due to weather patterns and soil

properties, and the combination of these, with the increase

in the level of air, water, and soil pollutants, and the effects

of climate change, could cause different types of MFSCs

that will severely decrease yield (Pascual et al., 2022; Zan-

dalinas, Fritschi, et al., 2021; Zandalinas & Mittler, 2022).

As agroecosystems mostly relay on a single prime species,

they are also highly prone to pathogen or insect attacks

that could decimate crops and severely decrease yield

(Zandalinas & Mittler, 2022). In this respect, two different

parameters could be playing a key role: (i) MFSCs could

weaken crops and decrease their overall resilience to insect

or pathogen attacks resulting in large outbreaks under the

current climate conditions; and (ii) The changing climate,

which could include warming trends and a potential

increase or decrease in precipitation in certain area of the

world, could promote the proliferation of particular patho-

gens and/or insects, increasing their initial burden and trig-

gering outbreaks. The very possible combination of these

Ó2023 Society for Experimental Biology and John Wiley & Sons Ltd.,

The Plant Journal, (2023), doi: 10.1111/tpj.16557

Multifactorial stress combination 9

two different scenarios/parameters could of course cause

massive outbreaks and yield declines leading to famine in

different areas, migration, and the destabilization of socie-

ties. The combined impact of water stress and insect her-

bivory, as observed in faba beans, was for example found

to reduce yield (Raderschall et al., 2021), and elevated tem-

peratures are known to increase the activity of different

crop pathogens (Cohen & Leach, 2020; Desaint et al., 2021;

Lehmann et al., 2020; Zarattini et al., 2021). A recent meta-

analysis further revealed that conditions such as high tem-

perature, increased CO

levels, drought, and/or nutrient

deﬁciencies led to increased herbivory consumption of

crops (Hamann, Blevins, et al., 2021).

While we may not currently observe or severely suffer

from the full effects of MFSC (Figures 1b and 6) on major

crops and their yield in large areas of our planet, the grad-

ually worsening environmental conditions, increasing pol-

lutant levels, and changes in the dynamics of pathogen

and insect populations, are likely to subject crops in larger

areas of our planet, in the near future, to MFSCs, causing

yield reductions. This risk should be anticipated and

addressed as its consequences could be highly severe to

our society. While addressing MFSC responses/resilience

using model plants and crops, we should be aware that

most lab and/or greenhouse studies of stress combina-

tion/MFSC to date fall short in addressing what really hap-

pens under ﬁeld conditions (e.g., Long & Ort, 2010; Mittler

& Blumwald, 2010). The use of pots for example limits the

soil volume the plant can use (Passioura, 2006), and

the light conditions/intensity/quality used, as well as tem-

perature changes, do not accurately reﬂect conditions in

the ﬁeld. Future studies of stress/stress combination/MFSC

should therefore attempt to use the ﬁeld environment as

much as possible. Although such studies are challenging,

as they require, for example, artiﬁcially enhancing soil,

water, and air levels of pollutants, they are highly needed.

An excellent example of ﬁeld studies of stress combina-

tions that involve elevated CO

levels is the studies con-

ducted using the Free-Air Carbon dioxide Enrichment

(FACE) settings, combined with drought/heat (e.g., Gilles-

pie et al., 2012; Ruiz-Vera et al., 2015; Thomey et al., 2019).

Below we will address some of the possible strategies that

could be used to enhance the resilience of crops to MFSC.

WHAT SHOULD WE DO NEXT?

The classical approach of introducing genes that enable

resilience to the environment or resistance to pathogens or

weeds via breeding and/or genetic engineering is based on

studies in which crops were subjected to one or at the

most two different stress conditions (Mittler & Blum-

wald, 2010; Rivero et al., 2022). While these studies may

currently be sufﬁcient to provide crops with protection

from the environment and maintain yield, they may not be

enough to mitigate the impacts of the more complex and

harsher MFSC environment of the near future; which could

subject plants and crops to a much more complex set of

stress combinations/MFSCs (Figure 1). As some of the

genes and genetic loci associated with tolerance to MFSC

in crops, such as soybean and rice, are only now beginning

to emerge (Pel

aez-Vico et al., 2023; Sinha, Pel

aez-Vico,

et al., 2023), very few target genes/loci for breeding and/or

genetic engineering are presently available. More studies

focused on the response and/or tolerance of different crops

to MFSC under ﬁeld conditions are therefore urgently

needed to identify these genes/loci. These studies should

be conducted in different regions of the world, tailored to

the different MFSCs that may occur there, and use ﬁeld

studies as much as possible, to mimic many of the

(a) (b)

100

150

200

250

300

Billion US dollars

Number of events

Drought Count Flooding Freeze Count Severe Storm Count

Tropical Cyclone Count Wildfire Count Winter Storm Count

Figure 6. Damages caused to US economy and agriculture as a result of global warming and climate change.

(a) Number of different weather events that caused damages exceeding a billion dollars each between 1980 and 2023. Note the increase in the frequency of

events in recent years.

(b) A sum of damages caused to US economy and agriculture from droughts, droughts combined with a heat wave, freeze, severe weather events, and ﬂoods,

between 1980 and 2023. Note the extent of damage caused by the combination of drought and a heat wave, compared to drought alone. Data was obtained

from The US National Centers for Environmental Information (https://www.ncei.noaa.gov/access/billions/).

Ó2023 Society for Experimental Biology and John Wiley & Sons Ltd.,

The Plant Journal, (2023), doi: 10.1111/tpj.16557

10 Sara I. Zandalinas et al.

predicted stress conditions/combinations that may arise in

these areas (Mittler, 2006; Mittler & Blumwald, 2010; Rivero

et al., 2022). In addition to directly testing the effects of

MFSC on currently cultivated crops, as described above,

large-scale genetic variability studies, using natural varie-

ties obtained from different regions around the world,

should also be conducted, as these would also help in

identifying genes/loci that may be associated with toler-

ance to MFSC. In a recent study, for example, 42 rice geno-

types were subjected to an MFSC of ﬁve different stresses

revealing that wild African rice (Wang et al., 2014) could be

a good source of genes to be used in enhancing MFSC

resilience in rice (Sinha, Pel

aez-Vico, et al., 2023). As recent

studies have shown that the responses, sensitivity, and tol-

erance of vegetative and reproductive tissues of plants to

stress/stress combination/MFSC could be very different

from each other (Pel

aez-Vico et al., 2023; Sinha et al., 2022;

Sinha, Induri, et al., 2023; Sinha, Shostak, et al., 2023), the

acclimation of both reproductive and vegetative tissues to

MFSC should be studied when conducting the different

molecular and genetic studies described above. In addi-

tion, strategies to alter the expression of large numbers

of transcripts in a tissue- and/or stress-speciﬁc manner

should be considered, as the molecular and physiological

responses of the different reproductive and vegetative tis-

sues and even their speciﬁc cell types could also be very

different from each other during stress combination/MFSC

(Pel

aez-Vico et al., 2023; Shaar-Moshe et al., 2017; Sinha

et al., 2022; Sinha, Induri, et al., 2023; Sinha, Shostak,

et al., 2023).

In addition to manipulating the plant genome to aug-

ment tolerance to MFSC, the resilience of the plant and

soil microbiomes should also be considered. MFSC was

recently shown to negatively impact microbiomes, and

these are critical for crop growth and yield in the ﬁeld (Ril-

lig et al., 2019; Rillig, Ryo, et al., 2021; Yang et al., 2021).

Future attempts to enhance the resilience of crops to MFSC

should therefore integrate the effects of MFSC on the plant

microbiome and its interactions with the plant, and even

attempt to use microbiomes that were hardened to resist

MFSC and could potentially be added/introduced at the

time of seed sowing. Rigorous methodology should how-

ever be applied in such studies (Ryan & Graham, 2018).

Other treatments that could be applied during sowing

(cheaper option) or at the seedlings, mature, or even ﬂow-

ering stages of crops, could be different stimulants that

enhance the tolerance of plants to stress. Of course, dedi-

cated studies focused on identifying speciﬁc chemical- or

bio-stimulants that enhance the tolerance of plants to

MFSC are needed before these approaches are attempted,

and the cost versus efﬁcacy of these treatments on overall

yield, in large acreage settings, need to be assessed.

As indicated above, current breeding efforts are

rooted in ﬁeld studies in which plants are subjected to the

natural environment that includes the potential combina-

tions of different stresses such as drought and heat, ﬂood-

ing and heat, and many other conditions. These efforts

resulted in the development of crop plants with high resil-

ience and plasticity to different stress conditions, able to

produce higher yields under our changing climate (e.g.,

cultivars that are indeterminate and can produce ﬂower-

s/seeds over a longer period that would overcome short

episodes of stress/stress combination). In addition, many

agricultural practices and strategies have been developed

to mitigate the effects of stress/stress combinations/climate

change (e.g., Anderson et al., 2020; Murrell, 2017).

Although these efforts are ongoing and would help in miti-

gating different conditions of stress/stress combinations

developing on our planet, they may not accurately antici-

pate the effects of new stress combinations/MFSCs that

could develop in the near future and involve combinations

of multiple low level stresses, some already known (e.g.,

water deﬁcit, heat, cold, ﬂooding), and some new and/or

unanticipated (e.g., increased levels of current, and/or new

types of air, water, and soil pollutants). Breeding and agri-

cultural practices urgently need therefore to address the

potential hazards of MFSCs (Figure 1b; Zandalinas, Fritschi,

et al., 2021; Zandalinas, Sengupta, et al., 2021; Zandalinas

& Mittler, 2022), so that we will not be surprised by them

and suffer major yield losses.

As global warming and climate change are predicted

to alter the types of crops we will be able to cultivate at dif-

ferent parts of our planet, and the growth regions/areas of

many crops would need to be ‘moved’ from certain loca-

tions to others, depending on the developing environmen-

tal conditions, the impacts of MFSC on these large crop

movements should also be assessed, especially in regions

that are closer to large industrial or urban areas; that may

introduce additional stressors in the form of pollution. The

effects of MFSCs on crops should also be incorporated into

the different agricultural practices currently applied in dif-

ferent regions of our planet, as well as into the different

models that affect the decisions of how to use these. In the

near future we may also have to be much more ﬂexible in

the types of crops we cultivate in different regions of our

planet, as well as be ready to dynamically change these

according to the developing conditions. As many econo-

mies worldwide may not be ready for such ‘plasticity’ in

large-scale crop cultivation, they might need to adjust to

be able to support their overall agricultural productivity

and economic stability.

The risk of not paying attention to the developing

environmental conditions on our planet and the higher

complexity they will impose on crops (i.e., MFSC; Figures 1

and 6) is high. If we will not strive to study MFSC and to

develop new crop varieties and agricultural practices that

increase resilient to it, we may experience unexpected,

rapid, and massive declines in yield that will affect large

Ó2023 Society for Experimental Biology and John Wiley & Sons Ltd.,

The Plant Journal, (2023), doi: 10.1111/tpj.16557

Multifactorial stress combination 11

areas of our planet and lead to the destabilizing of socie-

ties, famine, migration and even wars. Of particular impor-

tance to this concern is the fact that multiple ‘low’ level

stressors could cause a rapid decline in yield (i.e., the

MFSC principle; Figure 1b). We may not currently pay

attention therefore to low-level stressors in our environ-

ment, but as the number of these and their complexity

increases (i.e., MFSC), they could dramatically impact

plants and crops causing rapid and unexpected yield

reductions and ecosystem collapses. Studying MFSC is

therefore of high importance to our future!

Considering the high risk MFSC poses to our future,

and the unknown time it may take it to start impacting agri-

culture at a large scale (that may be already here, or very

soon), we need to be creative in our attempts to mitigate

it. For example, lifestyle properties of perennial plants

might need to be introduced into annual crops allowing

them to transiently slow metabolism during stress and

keep ﬂowering and producing seeds (as opposed to rapidly

transitioning into ﬂowering and seed set stages, followed

by dying; Mittler & Blumwald, 2010), a higher level of

ploidy might need to be introduced into crops (high levels

of ploidy is thought to have allowed land plants to survive

prior planet-wide disasters and weather changes; Cai

et al., 2019; Comai, 2005; Vanneste et al., 2014; Yao et al.,

2019), and combinations of strategies integrating technol-

ogy, engineering, and synthetic biology might need to be

developed to mitigate MFSC under ﬁeld conditions (Mittler

& Blumwald, 2010; Rivero et al., 2022; Zandalinas, Fritschi,

et al., 2021; Zandalinas & Mittler, 2022).

AUTHOR CONTRIBUTIONS

SIZ, MAP-V, RS, LSP, and RM wrote the manuscript.

ACKNOWLEDGMENTS

This work was supported by funding from the National Science

Foundation (IOS-2110017, IOS-1353886, IOS-1932639), Interdisci-

plinary Plant Group, and University of Missouri. LSP and SIZ

were supported by the contract PRE2022-101650 and RYC2020-

029967-I, respectively, funded by MCIN/AEI/10.13039/501100011033

and FSE+.

CONFLICT OF INTEREST

The authors declare no conﬂict of interest.

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Multifactorial stress combination 15

Identification of genes involved in the tomato root response to Globodera rostochiensis parasitism under varied light conditions

Preprint

Full-text available

Feb 2024

Understanding the intricate interplay between abiotic and biotic stresses is crucial for deciphering plant responses and developing resilient cultivars. Here, we investigate the combined effects of elevated light intensity and nematode infection on tomato seedlings. Chlorophyll fluorescence analysis revealed significant enhancements in PSII quantum yield and photochemical fluorescence quenching under high light conditions. qRT-PCR analysis of stress-related marker genes exhibited differential expression patterns in leaves and roots, indicating robust defense and antioxidant responses. Despite root protection from light, roots showed significant molecular changes, including down-regulation of genes associated with oxidative stress and up-regulation of genes involved in signalling pathways. Transcriptome analysis uncovered extensive gene expression alterations, with light exerting a dominant influence. Notably, light and nematode response synergistically induced more differentially expressed genes than individual stimuli. Functional categorization of differentially expressed genes upon double stimuli highlighted enrichment in metabolic pathways, biosynthesis of secondary metabolites, and amino acid metabolism, whereas the importance of specific pathogenesis related pathways decreased. Overall, our study elucidates complex plant responses to combined stresses, emphasizing the importance of integrated approaches for developing stress-resilient crops in the face of changing environmental conditions.

s00299-024-03153-7

Article

Feb 2024

Kadambot H M Siddique

Silicon and nitric oxide modulate growth attributes, antioxidant defense system and osmolytes accumulation in radish (Raphanus sativus L.) under arsenic toxicity

Article

Full-text available

May 2024

Plants adjust their developmental processes for their survival against changing environments. Plant development is adversely affected by arsenic (As) contamination. In order to mitigate As toxicity, the effect of silicon (Si) (as silicic acid) and nitric oxide (NO) (as sodium nitroprusside; SNP) was observed on 7 days old radish (Raphanus sativus L.) seedlings under 0.3, 0.5 and 0.7 mM As concentrations. Plant growth traits, oxidative stress, carbohydrates, protein, antioxidants and osmolytes were measured. Arsenic stress inhibited the growth parameters and caused oxidative damage by elevating the level of oxidative stress markers and by causing membrane and nuclear damage, as shown by histochemical studies. Activities of antioxidative enzymes, content of non-enzymatic antioxidants, and levels of osmolytes were also decreased by As stress. However, Si and NO supplementation enhanced the As tolerance by improving the plant growth parameters. Moreover, Si and NO application improved carbohydrates and protein contents and stimulated plant antioxidant defense systems by decreasing the level of malondialdehyde and hydrogen peroxide and by diminishing the membrane and nuclear damage caused by As. An increase in the osmolytes levels were observed by the application of Si and NO. Fourier transform infrared (FTIR) analysis showed that Si and NO exerted various peaks in different lipids, proteins, carbohydrates and cell wall component regions. This study suggests that Si and NO can help mitigating As-induced toxicity in R. sativus seedlings and augment growth.

Creating Climate-Resilient Crops by Increasing Drought, Heat, and Salt Tolerance

Article

Full-text available

Apr 2024

Over the years, the changes in the agriculture industry have been inevitable, considering the need to feed the growing population. As the world population continues to grow, food security has become challenged. Resources such as arable land and freshwater have become scarce due to quick urbanization in developing countries and anthropologic activities; expanding agricultural production areas is not an option. Environmental and climatic factors such as drought, heat, and salt stresses pose serious threats to food production worldwide. Therefore, the need to utilize the remaining arable land and water effectively and efficiently and to maximize the yield to support the increasing food demand has become crucial. It is essential to develop climate-resilient crops that will outperform traditional crops under any abiotic stress conditions such as heat, drought, and salt, as well as these stresses in any combinations. This review provides a glimpse of how plant breeding in agriculture has evolved to overcome the harsh environmental conditions and what the future would be like.

Elevated [CO2] and temperature augment gas exchange and shift the fitness landscape in a montane forb

Article

Full-text available

Apr 2024
NEW PHYTOL

Climate change is simultaneously increasing carbon dioxide concentrations ([CO2]) and temperature. These factors could interact to influence plant physiology and performance. Alternatively, increased [CO2] may offset costs associated with elevated temperatures. Furthermore, the interaction between elevated temperature and [CO2] may differentially affect populations from along an elevational gradient and disrupt local adaptation. We conducted a multifactorial growth chamber experiment to examine the interactive effects of temperature and [CO2] on fitness and ecophysiology of diverse accessions of Boechera stricta (Brassicaceae) sourced from a broad elevational gradient in Colorado. We tested whether increased [CO2] would enhance photosynthesis across accessions, and whether warmer conditions would depress the fitness of high‐elevation accessions owing to steep reductions in temperature with increasing elevation in this system. Elevational clines in [CO2] are not as evident, making it challenging to predict how locally adapted ecotypes will respond to elevated [CO2]. This experiment revealed that elevated [CO2] increased photosynthesis and intrinsic water use efficiency across all accessions. However, these instantaneous responses to treatments did not translate to changes in fitness. Instead, increased temperatures reduced the probability of reproduction for all accessions. Elevated [CO2] and increased temperatures interacted to shift the adaptive landscape, favoring lower elevation accessions for the probability of survival and fecundity. Our results suggest that elevated temperatures and [CO2] associated with climate change could have severe negative consequences, especially for high‐elevation populations.

Impact of Biotic/Abiotic Stress Factors on Plant Specialized Metabolites

Article

Full-text available

May 2024
INT J MOL SCI

Plants are a group of organisms that have developed remarkable adaptations to merely exist in the environment [...]

ROS are universal cell-to-cell stress signals

Article

Apr 2024

Redox Regulation by Priming Agents Toward a Sustainable Agriculture

Article

Mar 2024
PLANT CELL PHYSIOL

Plant are sessile organisms that are often subjected to a multitude of environmental stresses, with the occurrence of these events being further intensified by global climate change. Crop species therefore require specific adaptations to tolerate climatic variability for sustainable food production. Plant stress results in excess accumulation of reactive oxygen species (ROS) leading to oxidative stress, and loss of cellular redox balance in the plant cells. Moreover, enhancement of cellular oxidation as well as oxidative signals have recently been recognized as crucial players in plant growth regulation under stress conditions. Multiple roles of redox regulation in crop production have been well documented, and major emphasis has focused on key redox-regulated proteins and non-protein molecules, such as NAD(P)H, thioredoxins, glutathione, glutaredoxins, peroxiredoxins, ascorbate, and reduced ferredoxin. These have been widely implicated in the regulation of (epi)genetic factors modulating growth and vigor of crop plants, particularly within an agricultural context. In this regard, priming with the employment of chemical and biological agents has emerged as a fascinating approach to improve plant tolerance against various abiotic and biotic stressors. Priming in plants is a physiological process, where prior exposure to specific stressors induces a state of heightened alertness, enabling a more rapid and effective defense response upon subsequent encounters with similar challenges. Priming is reported to play an important role in the regulation of cellular redox homeostasis, maximizing crop productivity under stress conditions and thus achieving yield security. By taking this into consideration, the present review is an up-to-date critical evaluation of promising plant priming technologies and their role in the regulation of redox components towards enhanced plant adaptations to extreme unfavorable environmental conditions. The challenges and opportunities of plant priming are addressed, with the aim to encourage future research in this field towards effective application in crop stress management including horticultural species.

Stress combination: from genes to ecosystems

Article

Mar 2024
PLANT J

Transcriptomics, proteomics, and metabolomics interventions prompt crop improvement against metal(loid) toxicity

Article

Full-text available

Feb 2024
PLANT CELL REP

The escalating challenges posed by metal(loid) toxicity in agricultural ecosystems, exacerbated by rapid climate change and anthropogenic pressures, demand urgent attention. Soil contamination is a critical issue because it significantly impacts crop productivity. The widespread threat of metal(loid) toxicity can jeopardize global food security due to contaminated food supplies and pose environmental risks, contributing to soil and water pollution and thus impacting the whole ecosystem. In this context, plants have evolved complex mechanisms to combat metal(loid) stress. Amid the array of innovative approaches, omics, notably transcriptomics, proteomics, and metabolomics, have emerged as transformative tools, shedding light on the genes, proteins, and key metabolites involved in metal(loid) stress responses and tolerance mechanisms. These identified candidates hold promise for developing high-yielding crops with desirable agronomic traits. Computational biology tools like bioinformatics, biological databases, and analytical pipelines support these omics approaches by harnessing diverse information and facilitating the mapping of genotype-to-phenotype relationships under stress conditions. This review explores: (1) the multifaceted strategies that plants use to adapt to metal(loid) toxicity in their environment; (2) the latest findings in metal(loid)-mediated transcriptomics, proteomics, and metabolomics studies across various plant species; (3) the integration of omics data with artificial intelligence and high-throughput phenotyping; (4) the latest bioinformatics databases, tools and pipelines for single and/or multi-omics data integration; (5) the latest insights into stress adaptations and tolerance mechanisms for future outlooks; and (6) the capacity of omics advances for creating sustainable and resilient crop plants that can thrive in metal(loid)-contaminated environments.

Earth beyond six of nine planetary boundaries

Article

Full-text available

Sep 2023

This planetary boundaries framework update finds that six of the nine boundaries are transgressed, suggesting that Earth is now well outside of the safe operating space for humanity. Ocean acidification is close to being breached, while aerosol loading regionally exceeds the boundary. Stratospheric ozone levels have slightly recovered. The transgression level has increased for all boundaries earlier identified as overstepped. As primary production drives Earth system biosphere functions, human appropriation of net primary production is proposed as a control variable for functional biosphere integrity. This boundary is also transgressed. Earth system modeling of different levels of the transgression of the climate and land system change boundaries illustrates that these anthropogenic impacts on Earth system must be considered in a systemic context.

Climate trends and soybean production since 1970 in Mississippi: Empirical evidence from ARDL model

Article

Full-text available

Sep 2023
SCI TOTAL ENVIRON

When drought meets heat – a plant omics perspective

Article

Full-text available

Aug 2023

Changes in weather patterns with emerging drought risks and rising global temperature are widespread and negatively affect crop growth and productivity. In nature, plants are simultaneously exposed to multiple biotic and abiotic stresses, but most studies focus on individual stress conditions. However, the simultaneous occurrence of different stresses impacts plant growth and development differently than a single stress. Plants sense the different stress combinations in the same or in different tissues, which could induce specific systemic signalling and acclimation responses; impacting different stress-responsive transcripts, protein abundance and modifications, and metabolites. This mini-review focuses on the combination of drought and heat, two abiotic stress conditions that often occur together. Recent omics studies indicate common or independent regulators involved in heat or drought stress responses. Here, we summarize the current research results, highlight gaps in our knowledge, and flag potential future focus areas.

Evaluating the role of bacterial diversity in supporting soil ecosystem functions under anthropogenic stress

Article

Full-text available

Jul 2023

Ecosystem functions and services are under threat from anthropogenic global change at a planetary scale. Microorganisms are the dominant drivers of nearly all ecosystem functions and therefore ecosystem-scale responses are dependent on responses of resident microbial communities. However, the specific characteristics of microbial communities that contribute to ecosystem stability under anthropogenic stress are unknown. We evaluated bacterial drivers of ecosystem stability by generating wide experimental gradients of bacterial diversity in soils, applying stress to the soils, and measuring responses of several microbial-mediated ecosystem processes, including C and N cycling rates and soil enzyme activities. Some processes (e.g., C mineralization) exhibited positive correlations with bacterial diversity and losses of diversity resulted in reduced stability of nearly all processes. However, comprehensive evaluation of all potential bacterial drivers of the processes revealed that bacterial α diversity per se was never among the most important predictors of ecosystem functions. Instead, key predictors included total microbial biomass, 16S gene abundance, bacterial ASV membership, and abundances of specific prokaryotic taxa and functional groups (e.g., nitrifying taxa). These results suggest that bacterial α diversity may be a useful indicator of soil ecosystem function and stability, but that other characteristics of bacterial communities are stronger statistical predictors of ecosystem function and better reflect the biological mechanisms by which microbial communities influence ecosystems. Overall, our results provide insight into the role of microorganisms in supporting ecosystem function and stability by identifying specific characteristics of bacterial communities that are critical for understanding and predicting ecosystem responses to global change.

Effect of global warming on the potential distribution of a holoparasitic plant (Phelypaea tournefortii): both climate and host distribution matter

Article

Full-text available

Jul 2023

Phelypaea tournefortii (Orobanchaceae) primarily occurs in the Caucasus (Armenia, Azerbaijan, Georgia, and N Iran) and Turkey. This perennial, holoparasitic herb is achlorophyllous and possesses one of the most intense red flowers among all plants worldwide. It occurs as a parasite on the roots of several Tanacetum (Asteraceae) species and prefers steppe and semi-arid habitats. Climate change may affect holoparasites both directly through effects on their physiology and indirectly as a consequence of its effects on their host plants and habitats. In this study, we used the ecological niche modeling approach to estimate the possible effects of climate change on P. tournefortii and to evaluate the effect of its parasitic relationships with two preferred host species on the chances of survival of this species under global warming. We used four climate change scenarios (SSP1-2.6, SSP2-4.5, SSP3-7.0, SSP5-8.5) and three different simulations (CNRM, GISS-E2, INM). We modeled the species’ current and future distribution using the maximum entropy method implemented in MaxEnt using seven bioclimatic variables and species occurrence records (Phelypaea tournefortii – 63 records, Tanacetum argyrophyllum – 40, Tanacetum chiliophyllum – 21). According to our analyses, P. tournefortii will likely contract its geographical range remarkably. In response to global warming, the coverage of the species’ suitable niches will decrease by at least 34%, especially in central and southern Armenia, Nakhchivan in Azerbaijan, northern Iran, and NE Turkey. In the worst-case scenario, the species will go completely extinct. Additionally, the studied plant's hosts will lose at least 36% of currently suitable niches boosting the range contraction of P. tournefortii. The GISS-E2 scenario will be least damaging, while the CNRM will be most damaging to climate change for studied species. Our study shows the importance of including ecological data in niche models to obtain more reliable predictions of the future distribution of parasitic plants.

Jasmonic acid is required for tomato acclimation to multifactorial stress combination

Article

Full-text available

Jun 2023
ENVIRON EXP BOT

As a result of global warming and climate change, the number and intensity of weather events such as droughts, heat waves, and floods are increasing, resulting in major losses in crop yield worldwide. Combined with the accumulation of different pollutants, this situation is leading to a gradual increase in the complexity of environmental factors affecting plants. We recently used the term ‘multifactorial stress combination’ (MFSC) to describe the impact of three or more stressors occurring simultaneously or sequentially on plants. Here, we show that a MFSC of six different abiotic stressors (high light, heat, nitrogen deficiency, paraquat, cadmium, and salinity) has a negative impact on the growth, photosystem II function, and photosynthetic activity of mature tomato plants. We further reveal a negative correlation between proline accumulation and the increasing number of stress factors combined, suggesting that proline could have an adverse effect on plants during MFSC. Our findings further indicate that alterations in hormonal levels and stomatal responses are stress/stress combination-dependent, and that a tomato mutant deficient in jasmonic acid accumulation is more sensitive to high light and its combinations with salinity and/or paraquat. Taken together, our study reveals that the effects of MFSC on tomato plants are broad, that photosynthesis and proline accumulation are especially vulnerable to MFSC, and that jasmonic acid is required for tomato acclimation to MFSCs involving high light, salinity and paraquat.

A demographic approach for predicting population responses to multifactorial stressors

Article

Full-text available

Jun 2023

Meredith Zettlemoyer

Populations face a suite of anthropogenic stressors acting simultaneously, which can combine additively or interact to have complex effects on population persistence. Yet we still know relatively little about the mechanisms underlying population-level responses to multifactorial combinations of stressors because multiple stressor impacts across organisms' life cycles have not been systematically considered in population models. Specifically, different anthropogenic stressors can have variable effects across an organism's life cycle, resulting in non-intuitive results for long-term population persistence. For example, synergistic or antagonistic interactions might exacerbate or alleviate the effects of stressors on population dynamics, and different life-history stages or vital rates might contribute unequally to long-term population growth rates. Demographic modelling provides a framework to incorporate individual vital rate responses to multiple stressors into estimates of population growth, which will allow us to make more informed predictions about population-level responses to novel combinations of anthropogenic change. Without integrating stressors' interactive effects across the entire life cycle on population persistence, we may over- or underestimate threats to biodiversity and risk missing conservation management actions that could reduce species' vulnerability to stress.

The effects of multifactorial stress combination on rice and maize

Article

Oct 2023
PLANT PHYSIOL

The complexity of environmental factors affecting crops in the field is gradually increasing due to climate change-associated weather events, such as droughts or floods combined with heat waves, coupled with the accumulation of different environmental and agricultural pollutants. The impact of multiple stress conditions on plants was recently termed ‘multifactorial stress combination’ (MFSC) and defined as the occurrence of three or more stressors that impact plants simultaneously or sequentially. We recently reported that with the increased number and complexity of different MFSC stressors, the growth and survival of Arabidopsis (Arabidopsis thaliana) seedlings declines, even if the level of each individual stress is low enough to have no significant effect on plants. However, whether MFSC would impact commercial crop cultivars is largely unknown. Here, we reveal that a MFSC of 5 different low-level abiotic stresses (salinity, heat, the herbicide paraquat, phosphorus deficiency, and the heavy metal cadmium), applied in an increasing level of complexity, has a significant negative impact on the growth and biomass of a commercial rice (Oryza sativa) cultivar and a maize (Zea mays) hybrid. Proteomics, element content, and mixOmics analyses of MFSC in rice identified proteins that correlate with the impact of MFSC on rice seedlings, and analysis of 42 different rice genotypes subjected to MFSC revealed substantial genetic variability in responses to this unique state of stress combination. Taken together, our findings reveal that the impacts of MFSC on two different crop species are severe and that MFSC may substantially affect agricultural productivity.

A general concept of quantitative abiotic stress sensing

Article

Aug 2023

Plants often encounter stress in their environment. For appropriate responses to particular stressors, cells rely on sensory mechanisms that detect emerging stress. Considering sensor and signal amplification characteristics, a single sensor system hardly covers the entire stress range encountered by plants (e.g., salinity, drought, temperature stress). A dual system comprising stress-specific sensors and a general quantitative stress sensory system is proposed to enable the plant to optimize its response. The quantitative stress sensory system exploits the redox and reactive oxygen species (ROS) network by altering the oxidation and reduction rates of individual redox-active molecules under stress impact. The proposed mechanism of quantitative stress sensing also fits the requirement of dealing with multifactorial stress conditions.

Integrative phenotypic-transcriptomic analysis of soybean plants subjected to multifactorial stress combination

Preprint

Aug 2023

Global warming, climate change, and industrial pollution are altering our environment subjecting crops to an increasing number and complexity of abiotic stress conditions, concurrently or sequentially. Recent studies revealed that a combination of 3 or more stresses simultaneously impacting a plant (termed multifactorial stress combination; MFSC) can cause a drastic decline in plant growth and survival, even if the level of each stress involved in the MFSC has a negligible effect on plants. However, the impacts of MFSC on crops are largely unknown. We subjected soybean plants to a MFSC of up to five different stresses (water deficit, salinity, low phosphate, acidity, and cadmium), in an increasing level of complexity, and conducted integrative transcriptomic-phenotypic analysis of reproductive and vegetative tissues. We reveal that MFSC has a negative cumulative effect on soybean yield, that each set of MFSC condition elicits a unique transcriptomic response (that is different between flowers and leaves), and that selected genes expressed in leaves or flowers are linked to the effects of MFSC on different vegetative, physiological, and/or reproductive parameters. We further reveal that the transcriptomic response of soybean and Arabidopsis to MFSC shares common features associated with reactive oxygen and iron/copper signaling/metabolism. Our study provides unique phenotypic and transcriptomic datasets for dissecting the mechanistic effects of MFSC on the vegetative, physiological, and reproductive processes of a crop plant.

The impact of multifactorial stress combination on plants, crops, and ecosystems: How should we prepare for what comes next?

Abstract

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