Translational insights into abiotic interactions: From Arabidopsis to crop plants

Abstract

Understanding crop plants responses to abiotic stress is increasingly important in this changing climate. We asked experts how discoveries in Arabidopsis thaliana have translated into advancements in abiotic crop stress resilience. The theme is that core regulatory networks identified in Arabidopsis are conserved in crops, but the molecular regulation varies among species. For cold tolerance, the regulatory framework is conserved, but MAP Kinase signaling promotes degradation of the INDUCER OF DREB1 EXPRESSION transcription factor in Arabidopsis but inhibits it in rice. For hypoxia, manipulation of the oxygen sensing Arg/N-degron pathway discovered in Arabidopsis has improved waterlogging and flood tolerance in barley, maize, wheat, and soybean. For light signaling, overexpression of PHYTOCHROME B reduces shade avoidance, improving yield under dense planting in potato, soybean, and maize. In rice, understanding of nitrogen responsiveness, uptake, and transport in Arabidopsis has inspired engineering of the NRT1 nitrate transceptor to increase yield. Arabidopsis research has provided leads for genetic manipulations that may improve drought resilience in crop species. Growing plants in space generates a complex array of stresses, and Arabidopsis experiments in the space station prepare for future development of robust crops as integral components of the life support systems. For environmental regulation of flowering time, the role of the GIGANTEA - CONTANS - FLOWERING LOCUS T module elucidated in Arabidopsis is largely conserved in crop plants, although additional regulators modify short-day responsiveness in rice, soybean, chrysanthemum, and potato.

Figure 1.

Genetic regulation of cold tolerance in Arabidopsis and major crops. A) Overview of the current understanding of the DREB1 regulatory network in Arabidopsis. Both positive and negative regulators that modulate DREB1 expression and/or protein stability through various mechanisms are depicted. B) Key genetic components identified in various crops, including homologous genes, natural variations, and loci associated with cold adaptation. These elements represent promising targets for genetic manipulation aimed at mitigating the trade-offs between yield and stress tolerance in the development of cold-tolerant crop varieties.

Figure 2.

Arabidopsis research has yielded groundbreaking insights into plant low-oxygen sensing, signaling, and response in both developmental and environmental contexts. A) Schematic representation of the PLANT CYSTEINE OXIDASE (PCO) branch of the N-degron pathway and its current known substrates. ATE, arginyl transferase; MetAP, methionine amino-peptidase; PRT6, proteolysis 6; ^oxCys, oxidized cysteine. The oxygen and possible nitric oxide (NO) positions in the pathway are shown. Oxygen is used by PCOs to oxidize amino-terminal Cys of the substrates. B) The different aspects of hypoxia. Arabidopsis studies have been instrumental in our current understanding of how plants deal with environment-induced and developmental hypoxia. Stressful hypoxia (right side panel) occurs in the roots of waterlogged plants or shoots of plants during complete submergence in turbid flood waters. Impaired gas diffusion in water also causes a rapid rise in ethylene in flooded tissues. Oxygen and ethylene sensing and signaling pathways are part of a complex molecular network essential for plant responses to abiotic stress–induced hypoxia. Nonstressful hypoxia (left side panel) corresponds to hypoxic niches that affect plant development. Soil oxygen content can vary from 3% to 15% depending on soil type, depth, and compactness, whereas SAMs maintain 3% to 6% O₂. Flowering plants grow on an altitudinal range from sea level (pO₂ 21%) up to 6,000 meters above sea level (pO₂ 10%).

Figure 3.

Plant responses to light cues modified by crop management practices significantly influence key agronomic traits, and Arabidopsis research has been instrumental in identifying the crucial genetic players involved. In dense stands, shade perceived by photoreceptors (PHYB, CRY1, PHYA) triggers architectural changes that modulate crowding tolerance. The photo period, determined by location (latitude) and sowing date, influences flowering time and cycle length, depending on genes involved in light signaling and in some cases interacting with the circadian clock (PHYC, PRR7, GI, LNK2, ELF3). These changes in crowding tolerance and cycle length ultimately determine the optimal population density, sowing dates, and suitable locations for crop cultivation. The light signaling genes identified in Arabidopsis are highlighted in white boxes.

Figure 4.

Deciphering nitrogen (N) nutrition and signaling in Arabidopsis contributes to improve yield and NUE in crops. The main N sources in plant nutrition are the 2 inorganic forms nitrate (NO₃⁻) and ammonium (NH₄⁺). In Arabidopsis, molecular mechanisms associated with their perception, uptake, transport, remobilization, and assimilation have been deciphered. In rice, it is mainly the overexpression of homolog genes that led to increase yield and NUE. Regulators, such as transcription factors, are also promising targets as potential coordinators of the different steps of N journey in plants. Making root systems more efficient at capturing nutrients by optimizing the architecture is another interesting avenue.

Figure 5.

Approaches and targets toward improved drought resilience. Popular techniques for identifying and assessing candidate genes include GWAS, TWAS, inducible and clustered regularly interspaced short palindromic repeats (CRISPR)-targeted gene regulation, chemical genetics, and single-cell RNA sequencing. Advanced techniques for assessing drought response phenotypes include hyperspectral and thermal imaging and imaging rhizotrons. Gene targets for enhancing drought tolerance and/or avoidance in Arabidopsis are associated with xylem anatomy, stomatal kinetics and/or density, stress signaling pathways, and root architecture. Candidates indicated with OE (overexpression) or KO (knockout) were shown to confer improved drought phenotypes after that manipulation. Of the gene targets in this figure, only CspB from Bacillus subtilis and HaHD4 from sunflower have been incorporated into commercial crop lines; however, several candidate genes that regulate stomatal behavior or reduce stomatal density upon manipulation in Arabidopsis have produced favorable drought-related phenotypes upon manipulation of a related gene in crop species.

Figure 6.

The unique stresses of living in space. Spaceflight imposes a series of novel factors that biology must adapt to. These include the biological effects of reduced gravity (microgravity) on physiology and development (such as altered gravity-responsive growth) and microgravity's physical effects on the growth environment (such as loss of convection and increased impact of the adhesion of water) and increased radiation exposure. The space vehicle itself imposes other challenges such as constraints on physical space for plant growth and often an elevated CO₂ level (that can reach several thousands of ppm from crew respiration) along with a potentially complex environment of volatiles arising from outgassing from the plastics and polymers of the vehicle's construction.

Figure 7.

Overview of flowering regulation in Arabidopsis (LD model plant) and its parallels in SD crops: soybean (Glycine max), Chrysanthemum (Chrysanthemum seticuspe), and the tuberization pathway in potato (Solanum tuberosum). In Arabidopsis, central flowering regulators include the circadian clock and the interplay of florigens and antiflorigens to regulate flowering. Under LD photoperiods, the CO transcription factor activates FT expression. The FT protein moves from the leaves to the shoot apex, where it forms the Flowering Activation Complex (FAC) to initiate flowering. These regulators are conserved in SD crops, where they play critical roles in photoperiodic flowering, temperature-responsive flowering, and tuberization pathways. SD plants have evolved additional negative or antiflorigenic regulators (GmFT1a/4a in soybean, CsAFT in chrysanthemum, and StSP5G in potato) that suppress flowering and tuberization signals under LD or NB conditions or warm temperature.