Grain under pressure: Harnessing biochemical pathways to beat drought and heat in wheat

Abstract

Erratic climate patterns represent a remarkable challenge to global food security, particularly affecting staple cereal crops of which wheat (Triticum aestivum) plays a critical role in annual agricultural production globally. It has been shown that over the last four decades, wheat cultivation has faced an escalating vulnerability to a variety of abiotic stresses, including heat and drought. These stressors not only decrease overall yield but also compromise grain quality, leading to reduced soluble starch content, higher protein content, altered grain texture, diminished end-use quality, and various other undesirable changes. With climate change projections indicating an intensification and higher frequency of heat and drought conditions in the future, urgent action is needed to develop resilient wheat varieties. Achieving this goal relies on a comprehensive understanding of the molecular responses to environmental shifts during successive stages of reproduction. Here we discuss three types of critical biochemical pathways responsible for sustaining starch biosynthesis in both source and sink tissues under adverse environmental conditions during grain development: (i) signaling network and cross-talk between ABA and SnRK pathways; (ii) transcriptional changes of the enzymes and signaling components; and (iii) inhibition of enzyme activity through temperature-induced misfolding. While summarizing the current knowledge, we also highlight critical factors contributing to the deterioration of grain quality and propose potential strategies for enhancing the resilience of starch biosynthesis in wheat grain.

Keywords: abiotic stress; biochemical pathways; drought; grain development; heat; starch biosynthesis; wheat.

Figure 1

Heat and drought affect grain quality. (a) Nutrients in wheat grain. (b) Effects of heat and drought on wheat and grain quality. Created with BioRender.com.

Figure 2

Schematic illustrating starch synthesis reactions in cereal source and sink tissue. (a) Sucrose is produced in source tissues and then transported by SWEETs/SUTs transporters into the phloem for delivery to sink tissues. Sucrose controls its production by inhibiting trehalose‐6‐phosphate (T‐6‐P) phosphatase, which inhibits sucrose synthase. Sucrose non‐fermenting‐1‐related protein kinases (SnRKs) play a key role by either directly or indirectly interacting with the ABA signaling pathway to activate transcription factors bZIPs or AREB/ABFs, respectively, for T‐6‐P phosphatase production. SnRKs influence the flux of sucrose into the sink tissues by regulating SWEETs/SUTs expression. (b) In the sink tissue, the sucrose gives rise to glucose‐6‐phosphate through the activity of invertase and hexokinase. Conversion of glucose‐6‐phosphate into glucose‐1‐phosphate by phosphoglucomutase initiates the starch synthesis pathway. Glucose‐1‐phosphate is transported into the amyloplast, where it becomes amylose via APGase. Starch is produced from amylose by the starch‐branching enzymes. Black arrows represent the general flow of the pathway. Red arrows represent potential upregulation, and blue lines show potential inhibition. Enzymes and proteins are highlighted in green, and metabolites are highlighted in blue. The red block icon shows that the PP2Cs are not interacting with SnRKs in the presence of ABA, rendering the SnRKs active. ABFs, ABA‐responsive elements binding factors; bZIP, basic leucine zipper family of transcription factors; PP2Cs, A type 2C protein phosphatases; PYL, Pyrabactin resistance 1 (PYR1)/PYR1‐like receptor protein; SnRKs, sucrose non‐fermenting 1‐related kinases; SUT, sugar transporter/sugar carrier; SWEET, sugars will eventually be exported transporter; TPP, trehalose‐6‐phosphate phosphatase; TPS, trehalose‐6‐phosphate synthase. Created with BioRender.com.

Figure 3

Regulation of AGPase activity. (1) In the dark, AGPase exists as an inactive heterotetramer formed by disulfide bonds between the small subunits. Under light conditions, thioredoxins activate AGPase by breaking the disulfide bonds. Active AGPase heterodimers can be allosterically activated through (2) increased affinity for substrates caused by high levels of 3PGA and Fru6P and (3) phosphorylation. (4) High levels of orthophosphate can inactivate AGPase activity. 3PGA, 3‐phosphoglyceric acid; Fru6P, fructose‐6‐Phosphate; Glu1P, glucose‐1‐phosphate; LS, large subunit; SS, small subunit. Figure created with BioRender.com.

Figure 4

Abscisic acid (ABA) biosynthetic pathway in plants. ABA is synthesized de novo in the plastids from a C40 epoxy carotenoid precursor. The initial intermediates originating from glycolysis products, pyruvate, and glyceraldehyde‐3‐phosphate to isopentenyl diphosphate via the Methyl Erythritol Phosphate pathway are not depicted here. The C15 intermediate xanthoxin is converted into ABA through a two‐step reaction involving ABA‐aldehyde in the cytosol. The enzymes involved in ABA biosynthesis are highlighted in green ovals. Created with BioRender.com.