Sounds emitted by plants under stress are airborne and informative.

Stressed plants show altered phenotypes, including changes in color, smell, and shape. Yet, airborne sounds emitted by stressed plants have not been investigated before. Here we show that stressed plants emit airborne sounds that can be recorded from a distance and classified. We recorded ultrasonic sounds emitted by tomato and tobacco plants inside an acoustic chamber, and in a greenhouse, while monitoring the plant's physiological parameters. We developed machine learning models that succeeded in identifying the condition of the plants, including dehydration level and injury, based solely on the emitted sounds. These informative sounds may also be detectable by other organisms. This work opens avenues for understanding plants and their interactions with the environment and may have significant impact on agriculture.

Developmental Responses to Water and Salinity in Root Systems.

Roots provide the primary mechanism that plants use to absorb water and nutrients from their environment. These functions are dependent on developmental mechanisms that direct root growth and branching into regions of soil where these resources are relatively abundant. Water is the most limiting factor for plant growth, and its availability is determined by the weather, soil structure, and salinity. In this review, we define the developmental pathways that regulate the direction of growth and branching pattern of the root system, which together determine the expanse of soil from which a plant can access water. The ability of plants to regulate development in response to the spatial distribution of water is a focus of many recent studies and provides a model for understanding how biological systems utilize positional cues to affect signaling and morphogenesis. A better understanding of these processes will inform approaches to improve crop water use efficiency to more sustainably feed a growing population.

A viral small interfering RNA-host plant mRNA pathway modulates virus-induced drought tolerance by enhancing autophagy.

Virus-induced drought tolerance presents a fascinating facet of biotic-abiotic interaction in plants, yet its molecular intricacies remain unclear. Our study shows that cowpea mild mottle virus (CPMMV) infection enhances drought tolerance in common bean (Phaseolus vulgaris) plants through a virus-derived small interfering RNA (vsiRNA)-activated autophagy pathway. Specifically, a 21-bp vsiRNA originating from the CPMMV Triple Gene Block1 (TGB1) gene targeted the 5' untranslated region (UTR) of the host Teosinte branched 1, Cycloidea, Proliferating Cell Factor (TCP) transcription factor gene PvTCP2, independent of the known role of TGB1 as an RNA silencing suppressor. This targeting attenuated the expression of PvTCP2, which encodes a transcriptional repressor, and in turn upregulated the core autophagy-related gene (ATG) PvATG8c, leading to activated autophagy activity surpassing the level induced by drought or CPMMV infection alone. The downstream EARLY RESPONSIVE TO DEHYDRATION (ERD) effector PvERD15 is a homologue of Arabidopsis thaliana AtERD15, which positively regulates stomatal aperture. PvERD15 was degraded in PvATG8c-mediated autophagy. Therefore, we establish a TGB1-PvTCP2-PvATG8c-PvERD15 module as a trans-kingdom fine-tuning mechanism that contributes to virus-induced drought tolerance in plant-drought-virus interactions.

Natural variation in response to combined water and nitrogen deficiencies in Arabidopsis.

Understanding plant responses to individual stresses does not mean that we understand real world situations, where stresses usually combine and interact. These interactions arise at different levels, from stress exposure to the molecular networks of the stress response. Here, we built an in-depth multi-omics description of plant responses to mild water (W) and nitrogen (N) limitations, either individually or combined, among five genetically different Arabidopsis (Arabidopsis thaliana) accessions. We highlight the different dynamics in stress response through integrative traits such as rosette growth and the physiological status of the plants. We also used transcriptomics and metabolomics profiling during a stage when the plant response was stabilized to determine the wide diversity in stress-induced changes among accessions, highlighting the limited reality of a 'universal' stress response. The main effect of the WxN interaction was an attenuation of the N-deficiency syndrome when combined with mild drought, but to a variable extent depending on the accession. Other traits subject to WxN interactions are often accession-specific. Multi-omics analyses identified a subset of transcript-metabolite clusters that are critical to stress responses but essentially variable according to the genotype factor. Including intra-specific diversity in our descriptions of plant stress response places our findings in perspective.

Extreme drought impacts have been underestimated in grasslands and shrublands globally.

Climate change is increasing the frequency and severity of short-term (~1 y) drought events-the most common duration of drought-globally. Yet the impact of this intensification of drought on ecosystem functioning remains poorly resolved. This is due in part to the widely disparate approaches ecologists have employed to study drought, variation in the severity and duration of drought studied, and differences among ecosystems in vegetation, edaphic and climatic attributes that can mediate drought impacts. To overcome these problems and better identify the factors that modulate drought responses, we used a coordinated distributed experiment to quantify the impact of short-term drought on grassland and shrubland ecosystems. With a standardized approach, we imposed ~a single year of drought at 100 sites on six continents. Here we show that loss of a foundational ecosystem function-aboveground net primary production (ANPP)-was 60% greater at sites that experienced statistically extreme drought (1-in-100-y event) vs. those sites where drought was nominal (historically more common) in magnitude (35% vs. 21%, respectively). This reduction in a key carbon cycle process with a single year of extreme drought greatly exceeds previously reported losses for grasslands and shrublands. Our global experiment also revealed high variability in drought response but that relative reductions in ANPP were greater in drier ecosystems and those with fewer plant species. Overall, our results demonstrate with unprecedented rigor that the global impacts of projected increases in drought severity have been significantly underestimated and that drier and less diverse sites are likely to be most vulnerable to extreme drought.

Critical slowing down of the Amazon forest after increased drought occurrence.

Dynamic ecosystems, such as the Amazon forest, are expected to show critical slowing down behavior, or slower recovery from recurrent small perturbations, as they approach an ecological threshold to a different ecosystem state. Drought occurrences are becoming more prevalent across the Amazon, with known negative effects on forest health and functioning, but their actual role in the critical slowing down patterns still remains elusive. In this study, we evaluate the effect of trends in extreme drought occurrences on temporal autocorrelation (TAC) patterns of satellite-derived indices of vegetation activity, an indicator of slowing down, between 2001 and 2019. Differentiating between extreme drought frequency, intensity, and duration, we investigate their respective effects on the slowing down response. Our results indicate that the intensity of extreme droughts is a more important driver of slowing down than their duration, although their impacts vary across the different Amazon regions. In addition, areas with more variable precipitation are already less ecologically stable and need fewer droughts to induce slowing down. We present findings indicating that most of the Amazon region does not show an increasing trend in TAC. However, the predicted increase in extreme drought intensity and frequency could potentially transition significant portions of this ecosystem into a state with altered functionality.

The nonlinear mechanics of highly extensible plant epidermal cell walls.

Plant epidermal cell walls maintain the mechanical integrity of plants and restrict organ growth. Mechanical analyses can give insights into wall structure and are inputs for mechanobiology models of plant growth. To better understand the intrinsic mechanics of epidermal cell walls and how they may accommodate large deformations during growth, we analyzed a geometrically simple material, onion epidermal strips consisting of only the outer (periclinal) cell wall, ~7 µm thick. With uniaxial stretching by >40%, the wall showed complex three-phase stress-strain responses while cyclic stretching revealed reversible and irreversible deformations and elastic hysteresis. Stretching at varying strain rates and temperatures indicated the wall behaved more like a network of flexible cellulose fibers capable of sliding than a viscoelastic composite with pectin viscosity. We developed an analytic framework to quantify nonlinear wall mechanics in terms of stiffness, deformation, and energy dissipation, finding that the wall stretches by combined elastic and plastic deformation without compromising its stiffness. We also analyzed mechanical changes in slightly dehydrated walls. Their extension became stiffer and more irreversible, highlighting the influence of water on cellulose stiffness and sliding. This study offers insights into the structure and deformation modes of primary cell walls and presents a framework that is also applicable to tissues and whole organs.

Mechanistic links between physiology and spectral reflectance enable previsual detection of oak wilt and drought stress.

Tree mortality due to global change-including range expansion of invasive pests and pathogens-is a paramount threat to forest ecosystems. Oak forests are among the most prevalent and valuable ecosystems both ecologically and economically in the United States. There is increasing interest in monitoring oak decline and death due to both drought and the oak wilt pathogen (Bretziella fagacearum). We combined anatomical and ecophysiological measurements with spectroscopy at leaf, canopy, and airborne levels to enable differentiation of oak wilt and drought, and detection prior to visible symptom appearance. We performed an outdoor potted experiment with Quercus rubra saplings subjected to drought stress and/or artificially inoculated with the pathogen. Models developed from spectral reflectance accurately predicted ecophysiological indicators of oak wilt and drought decline in both potted and field experiments with naturally grown saplings. Both oak wilt and drought resulted in blocked water transport through xylem conduits. However, oak wilt impaired conduits in localized regions of the xylem due to formation of tyloses instead of emboli. The localized tylose formation resulted in more variable canopy photosynthesis and water content in diseased trees than drought-stressed ones. Reflectance signatures of plant photosynthesis, water content, and cellular damage detected oak wilt and drought 12 d before visual symptoms appeared. Our results show that leaf spectral reflectance models predict ecophysiological processes relevant to detection and differentiation of disease and drought. Coupling spectral models that detect physiological change with spatial information enhances capacity to differentiate plant stress types such as oak wilt and drought.

Limited intraspecific variation in drought resistance along a pronounced tropical rainfall gradient.

Assessing within-species variation in response to drought is crucial for predicting species' responses to climate change and informing restoration and conservation efforts, yet experimental data are lacking for the vast majority of tropical tree species. We assessed intraspecific variation in response to water availability across a strong rainfall gradient for 16 tropical tree species using reciprocal transplant and common garden field experiments, along with measurements of gene flow and key functional traits linked to drought resistance. Although drought resistance varies widely among species in these forests, we found little evidence for within-species variation in drought resistance. For the majority of functional traits measured, we detected no significant intraspecific variation. The few traits that did vary significantly between drier and wetter origins of the same species all showed relationships opposite to expectations based on drought stress. Furthermore, seedlings of the same species originating from drier and wetter sites performed equally well under drought conditions in the common garden experiment and at the driest transplant site. However, contrary to expectation, wetter-origin seedlings survived better than drier-origin seedlings under wetter conditions in both the reciprocal transplant and common garden experiment, potentially due to lower insect herbivory. Our study provides the most comprehensive picture to date of intraspecific variation in tropical tree species' responses to water availability. Our findings suggest that while drought plays an important role in shaping species composition across moist tropical forests, its influence on within-species variation is limited.

LncRNA DANA1 promotes drought tolerance and histone deacetylation of drought responsive genes in Arabidopsis.

Although many long noncoding RNAs have been discovered in plants, little is known about their biological function and mode of action. Here we show that the drought-induced long intergenic noncoding RNA DANA1 interacts with the L1p/L10e family member protein DANA1-INTERACTING PROTEIN 1 (DIP1) in the cell nucleus of Arabidopsis, and both DANA1 and DIP1 promote plant drought resistance. DANA1 and DIP1 increase histone deacetylase HDA9 binding to the CYP707A1 and CYP707A2 loci. DIP1 further interacts with PWWP3, a member of the PEAT complex that associates with HDA9 and has histone deacetylase activity. Mutation of DANA1 enhances CYP707A1 and CYP707A2 acetylation and expression resulting in impaired drought tolerance, in agreement with dip1 and pwwp3 mutant phenotypes. Our results demonstrate that DANA1 is a positive regulator of drought response and that DANA1 works jointly with the novel chromatin-related factor DIP1 on epigenetic reprogramming of the plant transcriptome during the response to drought.

Climate change will accelerate the high-end risk of compound drought and heatwave events.

Compound drought and heatwave (CDHW) events have garnered increased attention due to their significant impacts on agriculture, energy, water resources, and ecosystems. We quantify the projected future shifts in CDHW characteristics (such as frequency, duration, and severity) due to continued anthropogenic warming relative to the baseline recent observed period (1982 to 2019). We combine weekly drought and heatwave information for 26 climate divisions across the globe, employing historical and projected model output from eight Coupled Model Intercomparison Project 6 GCMs and three Shared Socioeconomic Pathways. Statistically significant trends are revealed in the CDHW characteristics for both recent observed and model simulated future period (2020 to 2099). East Africa, North Australia, East North America, Central Asia, Central Europe, and Southeastern South America show the greatest increase in frequency through the late 21st century. The Southern Hemisphere displays a greater projected increase in CDHW occurrence, while the Northern Hemisphere displays a greater increase in CDHW severity. Regional warmings play a significant role in CDHW changes in most regions. These findings have implications for minimizing the impacts of extreme events and developing adaptation and mitigation policies to cope with increased risk on water, energy, and food sectors in critical geographical regions.

Cross-species predictive modeling reveals conserved drought responses between maize and sorghum.

Drought tolerance is a highly complex trait controlled by numerous interconnected pathways with substantial variation within and across plant species. This complexity makes it difficult to distill individual genetic loci underlying tolerance, and to identify core or conserved drought-responsive pathways. Here, we collected drought physiology and gene expression datasets across diverse genotypes of the C4 cereals sorghum and maize and searched for signatures defining water-deficit responses. Differential gene expression identified few overlapping drought-associated genes across sorghum genotypes, but using a predictive modeling approach, we found a shared core drought response across development, genotype, and stress severity. Our model had similar robustness when applied to datasets in maize, reflecting a conserved drought response between sorghum and maize. The top predictors are enriched in functions associated with various abiotic stress-responsive pathways as well as core cellular functions. These conserved drought response genes were less likely to contain deleterious mutations than other gene sets, suggesting that core drought-responsive genes are under evolutionary and functional constraints. Our findings support a broad evolutionary conservation of drought responses in C4 grasses regardless of innate stress tolerance, which could have important implications for developing climate resilient cereals.

Drought impacts on the electricity system, emissions, and air quality in the western United States.

The western United States has experienced severe drought in recent decades, and climate models project increased drought risk in the future. This increased drying could have important implications for the region's interconnected, hydropower-dependent electricity systems. Using power-plant level generation and emissions data from 2001 to 2021, we quantify the impacts of drought on the operation of fossil fuel plants and the associated impacts on greenhouse gas (GHG) emissions, air quality, and human health. We find that under extreme drought, electricity generation from individual fossil fuel plants can increase up to 65% relative to average conditions, mainly due to the need to substitute for reduced hydropower. Over 54% of this drought-induced generation is transboundary, with drought in one electricity region leading to net imports of electricity and thus increased pollutant emissions from power plants in other regions. These drought-induced emission increases have detectable impacts on local air quality, as measured by proximate pollution monitors. We estimate that the monetized costs of excess mortality and GHG emissions from drought-induced fossil generation are 1.2 to 2.5x the reported direct economic costs from lost hydro production and increased demand. Combining climate model estimates of future drying with stylized energy-transition scenarios suggests that these drought-induced impacts are likely to remain large even under aggressive renewables expansion, suggesting that more ambitious and targeted measures are needed to mitigate the emissions and health burden from the electricity sector during drought.

Dryland sensitivity to climate change and variability using nonlinear dynamics.

Primary productivity response to climatic drivers varies temporally, indicating state-dependent interactions between climate and productivity. Previous studies primarily employed equation-based approaches to clarify this relationship, ignoring the state-dependent nature of ecological dynamics. Here, using 40 y of climate and productivity data from 48 grassland sites across Mongolia, we applied an equation-free, nonlinear time-series analysis to reveal sensitivity patterns of productivity to climate change and variability and clarify underlying mechanisms. We showed that productivity responded positively to annual precipitation in mesic regions but negatively in arid regions, with the opposite pattern observed for annual mean temperature. Furthermore, productivity responded negatively to decreasing annual aridity that integrated precipitation and temperature across Mongolia. Productivity responded negatively to interannual variability in precipitation and aridity in mesic regions but positively in arid regions. Overall, interannual temperature variability enhanced productivity. These response patterns are largely unrecognized; however, two mechanisms are inferable. First, time-delayed climate effects modify annual productivity responses to annual climate conditions. Notably, our results suggest that the sensitivity of annual productivity to increasing annual precipitation and decreasing annual aridity can even be negative when the negative time-delayed effects of annual precipitation and aridity on productivity prevail across time. Second, the proportion of plant species resistant to water and temperature stresses at a site determines the sensitivity of productivity to climate variability. Thus, we highlight the importance of nonlinear, state-dependent sensitivity of productivity to climate change and variability, accurately forecasting potential biosphere feedback to the climate system.

Constitutively active B2 Raf-like kinases are required for drought-responsive gene expression upstream of ABA-activated SnRK2 kinases.

Osmotic stresses, such as drought and high salinity, adversely affect plant growth and productivity. The phytohormone abscisic acid (ABA) accumulates in response to osmotic stress and enhances stress tolerance in plants by triggering multiple physiological responses through ABA signaling. Subclass III SNF1-related protein kinases 2 (SnRK2s) are key regulators of ABA signaling. Although SnRK2s have long been considered to be self-activated by autophosphorylation after release from PP2C-mediated inhibition, they were recently revealed to be activated by two independent subfamilies of group B Raf-like kinases, B2-RAFs and B3-RAFs, under osmotic stress conditions. However, the relationship between SnRK2 phosphorylation by these RAFs and SnRK2 autophosphorylation and the individual physiological roles of each RAF subfamily remain unknown. In this study, we indicated that B2-RAFs are constantly active and activate SnRK2s when released from PP2C-mediated inhibition by ABA-binding ABA receptors, whereas B3-RAFs are activated only under stress conditions in an ABA-independent manner and enhance SnRK2 activity. Autophosphorylation of subclass III SnRK2s is not sufficient for ABA responses, and B2-RAFs are needed to activate SnRK2s in an ABA-dependent manner. Using plants grown in soil, we found that B2-RAFs regulate subclass III SnRK2s at the early stage of drought stress, whereas B3-RAFs regulate SnRK2s at the later stage. Thus, B2-RAFs are essential kinases for the activation of subclass III SnRK2s in response to ABA under mild osmotic stress conditions, and B3-RAFs function as enhancers of SnRK2 activity under severe stress conditions.

Metabolite-mediated adaptation of crops to drought and the acquisition of tolerance.

Drought is one of the major and growing threats to agriculture productivity and food security. Metabolites are involved in the regulation of plant responses to various environmental stresses, including drought stress. The complex drought tolerance can be ascribed to several simple metabolic traits. These traits could then be used for detecting the genetic architecture of drought tolerance. Plant metabolomes show dynamic differences when drought occurs during different developmental stages or upon different levels of drought stress. Here, we reviewed the major and most recent findings regarding the metabolite-mediated plant drought response. Recent progress in the development of drought-tolerant agents is also discussed. We provide an updated schematic overview of metabolome-driven solutions for increasing crop drought tolerance and thereby addressing an impending agricultural challenge.

Comprehensive assessment of drought resistance and recovery in kiwifruit genotypes using multivariate analysis.

As global climate change persists, ongoing warming exposes plants, including kiwifruit, to repeated cycles of drought stress and rewatering, necessitating the identification of drought-resistant genotypes for breeding purposes. To better understand the physiological mechanisms underlying drought resistance and recovery in kiwifruit, moderate (40-45% field capacity) and severe (25-30% field capacity) drought stresses were applied, followed by rewatering (80-85% field capacity) to eight kiwifruit rootstocks in this study. We then conducted a multivariate analysis of 20 indices for the assessment of drought resistance and recovery capabilities. Additionally, we identified four principal components, each playing a vital role in coping with diverse water conditions. Three optimal indicator groups were pinpointed, enhancing precision in kiwifruit drought resistance and recovery assessment and simplifying the evaluation system. Finally, MX-1 and HW were identified as representative rootstocks for future research on kiwifruit's responses to moderate and severe drought stresses. This study not only enhances our understanding of the response mechanisms of kiwifruit rootstocks to progressive drought stress and recovery but also provides theoretical guidance for reliable screening of drought-adaptive kiwifruit genotypes.

Testing the large genome constraint hypothesis in tropical rhizomatous herbs: life strategies, plant traits and habitat preferences in gingers.

Plant species with large genomes tend to be excluded from climatically more extreme environments with a shorter growing season. Species that occupy such environments are assumed to be under natural selection for more rapid growth and smaller genome size (GS). However, evidence for this is available only for temperate organisms. Here, we study the evolution of GS in two subfamilies of the tropical family Zingiberaceae to find out whether species with larger genomes are confined to environments where the vegetative season is longer. We tested our hypothesis on 337 ginger species from regions with contrasting climates by correlating their GS with an array of plant traits and environmental variables. We revealed 16-fold variation in GS which was tightly related to shoot seasonality. Negative correlations of GS with latitude, temperature and precipitation emerged in the subfamily Zingiberoidae, demonstrating that species with larger GS are excluded from areas with a shorter growing season. In the subfamily Alpinioideae, GS turned out to be correlated with the type of stem and light requirements and its members cope with seasonality mainly by adaptation to shady and moist habitats. The Ornstein-Uhlenbeck models suggested that evolution in regions with humid climates favoured larger GS than in drier regions. Our results indicate that climate seasonality exerts an upper constraint on GS not only in temperate regions but also in the tropics, unless species with large genomes find alternative ways to escape from that constraint.

Cotton GhNAC4 promotes drought tolerance by regulating secondary cell wall biosynthesis and ribosomal protein homeostasis.

Drought has a severe impact on the quality and yield of cotton. Deciphering the key genes related to drought tolerance is important for understanding the regulation mechanism of drought stress and breeding drought-tolerant cotton cultivars. Several studies have demonstrated that NAC transcription factors are crucial in the regulation of drought stress, however, the related functional mechanisms are still largely unexplored. Here, we identified that NAC transcription factor GhNAC4 positively regulated drought stress tolerance in cotton. The expression of GhNAC4 was significantly induced by abiotic stress and plant hormones. Silencing of GhNAC4 distinctly impaired the resistance to drought stress and overexpressing GhNAC4 in cotton significantly enhanced the stress tolerance. RNA-seq analysis revealed that overexpression of GhNAC4 enriched the expression of genes associated with the biosynthesis of secondary cell walls and ribosomal proteins. We confirmed that GhNAC4 positively activated the expressions of GhNST1, a master regulator reported previously in secondary cell wall formation, and two ribosomal protein-encoding genes GhRPL12 and GhRPL18p, by directly binding to their promoter regions. Overexpression of GhNAC4 promoted the expression of downstream genes associated with the secondary wall biosynthesis, resulting in enhancing secondary wall deposition in the roots, and silencing of GhRPL12 and GhRPL18p significantly impaired the resistance to drought stress. Taken together, our study reveals a novel pathway mediated by GhNAC4 that promotes secondary cell wall biosynthesis to strengthen secondary wall development and regulates the expression of ribosomal protein-encoding genes to maintain translation stability, which ultimately enhances drought tolerance in cotton.

Genome-wide mapping of DNase I hypersensitive sites revealed differential chromatin accessibility and regulatory DNA elements under drought stress in rice cultivars.

Drought stress (DS) is one of the major constraints limiting yield in crop plants including rice. Gene regulation under DS is largely governed by accessibility of the transcription factors (TFs) to their cognate cis-regulatory elements (CREs). In this study, we used DNase I hypersensitive assays followed by sequencing to identify the accessible chromatin regions under DS in a drought-sensitive (IR64) and a drought-tolerant (N22) rice cultivar. Our results indicated that DNase I hypersensitive sites (DHSs) were highly enriched at transcription start sites (TSSs) and numerous DHSs were detected in the promoter regions. DHSs were concurrent with epigenetic marks and the genes harboring DHSs in their TSS and promoter regions were highly expressed. In addition, DS induced changes in DHSs (∆DHSs) in TSS and promoter regions were positively correlated with upregulation of several genes involved in drought/abiotic stress response, those encoding TFs and located within drought-associated quantitative trait loci, much preferentially in the drought-tolerant cultivar. The CREs representing the binding sites of TFs involved in DS response were detected within the ∆DHSs, suggesting differential accessibility of TFs to their cognate sites under DS in different rice cultivars, which may be further deployed for enhancing drought tolerance in rice.