Plants are frequently subjected to different combinations of abiotic stresses, such as high light (HL) intensity, and elevated temperatures. These environmental conditions pose a threat to agriculture production, affecting photosynthesis, and decreasing yield. Metabolic responses of plants, such as alterations in carbohydrates and amino acid fluxes, play a key role in the successful acclimation of plants to different abiotic stresses, directing resources toward stress responses, and suppressing growth. Here we show that the primary metabolic response of Arabidopsis (Arabidopsis thaliana) plants to HL or heat stress (HS) is different from that of plants subjected to a combination of HL and HS (HL+HS). We further demonstrate that the combined stress results in a unique metabolic response that includes increased accumulation of sugars and amino acids coupled with decreased levels of metabolites participating in the tricarboxylic acid cycle. Among the amino acids exclusively accumulated during HL+HS, we identified the nonproteinogenic amino acid γ-aminobutyric acid (GABA). Analysis of different mutants deficient in GABA biosynthesis (GLUTAMATE DESCARBOXYLASE 3 [gad3]) as well as mutants impaired in autophagy (autophagy-related proteins 5 and 9 [atg5 and atg9]), revealed that GABA plays a key role in the acclimation of plants to HL+HS, potentially by promoting autophagy. Taken together, our findings identify a role for GABA in regulating plant responses to combined stress.
Climate change is predicted to increase the frequency and intensity of abiotic stress combinations that negatively impact plants and pose a serious threat to crop yield and food supply. Plants respond to episodes of stress combination by activating specific physiological and molecular responses, as well as by adjusting different metabolic pathways, to mitigate the negative effects of the stress combination on plant growth, development, and reproduction. Plants synthesize a wide range of metabolites that regulate many aspects of plant growth and development, as well as plant responses to stress. Although metabolic responses to individual abiotic stresses have been studied extensively in different plant species, recent efforts have been directed at understanding metabolic responses that occur when different abiotic factors are combined. In this review we examine recent studies of metabolomic changes under stress combination in different plants and suggest new avenues for the development of stress combination-resilient crops based on metabolites as breeding targets.
more » « less- Award ID(s):
- 2110017
- PAR ID:
- 10398166
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Experimental Botany
- Volume:
- 73
- Issue:
- 11
- ISSN:
- 0022-0957
- Format(s):
- Medium: X Size: p. 3339-3354
- Size(s):
- p. 3339-3354
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
null (Ed.)Extreme environmental conditions, such as heat, salinity, and decreased water availability, can have a devastating impact on plant growth and productivity, potentially resulting in the collapse of entire ecosystems. Stress-induced systemic signaling and systemic acquired acclimation play canonical roles in plant survival during episodes of environmental stress. Recent studies revealed that in response to a single abiotic stress, applied to a single leaf, plants mount a comprehensive stress-specific systemic response that includes the accumulation of many different stress-specific transcripts and metabolites, as well as a coordinated stress-specific whole-plant stomatal response. However, in nature plants are routinely subjected to a combination of two or more different abiotic stresses, each potentially triggering its own stress-specific systemic response, highlighting a new fundamental question in plant biology: are plants capable of integrating two different systemic signals simultaneously generated during conditions of stress combination? Here we show that plants can integrate two different systemic signals simultaneously generated during stress combination, and that the manner in which plants sense the different stresses that trigger these signals (i.e., at the same or different parts of the plant) makes a significant difference in how fast and efficient they induce systemic reactive oxygen species (ROS) signals; transcriptomic, hormonal, and stomatal responses; as well as plant acclimation. Our results shed light on how plants acclimate to their environment and survive a combination of different abiotic stresses. In addition, they highlight a key role for systemic ROS signals in coordinating the response of different leaves to stress.more » « less
-
more » « less
Abstract The growth, survival, and productivity of plants are constantly challenged by diverse abiotic stresses. When plants are exposed to stress for the first time, they can capture molecular information and store it as a form of memory, which enables them to competently and rapidly respond to subsequent stress(es). This process is referred to as a priming-induced or acquired stress response. In this review, we discuss how (i) the storage and retrieval of the information from stress memory modulates plant physiological, cellular, and molecular processes in response to subsequent stress(es), (ii) the intensity, recurrence, and duration of priming stimuli influences the outcomes of the stress response, and (iii) the varying responses at different plant developmental stages. We highlight current understanding of the distinct and common molecular processes manifested at the epigenetic, (post-)transcriptional, and post-translational levels mediated by stress-associated molecules and metabolites, including phytohormones. We conclude by emphasizing how unravelling the molecular circuitry underlying diverse priming-stimuli-induced stress responses could propel the use of priming as a management practice for crop plants. This practice, in combination with precision agriculture, could aid in increasing yield quantity and quality to meet the rapidly rising demand for food.
-
Plants often live in adverse environmental conditions and are exposed to various stresses, such as heat, cold, heavy metals, salt, radiation, poor lighting, nutrient deficiency, drought, or flooding. To adapt to unfavorable environments, plants have evolved specialized molecular mechanisms that serve to balance the trade-off between abiotic stress responses and growth. These mechanisms enable plants to continue to develop and reproduce even under adverse conditions. Ethylene, as a key growth regulator, is leveraged by plants to mitigate the negative effects of some of these stresses on plant development and growth. By cooperating with other hormones, such as jasmonic acid (JA), abscisic acid (ABA), brassinosteroids (BR), auxin, gibberellic acid (GA), salicylic acid (SA), and cytokinin (CK), ethylene triggers defense and survival mechanisms thereby coordinating plant growth and development in response to abiotic stresses. This review describes the crosstalk between ethylene and other plant hormones in tipping the balance between plant growth and abiotic stress responses.more » « less
-
more » « less
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 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.
