Sugar starvation-regulated MYBS2 and 14-3-3 protein interactions enhance plant growth, stress tolerance, and grain weight in rice

Abstract

Autotrophic plants have evolved distinctive mechanisms for maintaining a range of homeostatic states for sugars. The on/off switch of reversible gene expression by sugar starvation/provision represents one of the major mechanisms by which sugar levels are maintained, but the details remain unclear. α-Amylase (αAmy) is the key enzyme for hydrolyzing starch into sugars for plant growth, and it is induced by sugar starvation and repressed by sugar provision. αAmy can also be induced by various other stresses, but the physiological significance is unclear. Here, we reveal that the on/off switch of αAmy expression is regulated by 2 MYB transcription factors competing for the same promoter element. MYBS1 promotes αAmy expression under sugar starvation, whereas MYBS2 represses it. Sugar starvation promotes nuclear import of MYBS1 and nuclear export of MYBS2, whereas sugar provision has the opposite effects. Phosphorylation of MYBS2 at distinct serine residues plays important roles in regulating its sugar-dependent nucleocytoplasmic shuttling and maintenance in cytoplasm by 14-3-3 proteins. Moreover, dehydration, heat, and osmotic stress repress MYBS2 expression, thereby inducing αAmy3. Importantly, activation of αAmy3 and suppression of MYBS2 enhances plant growth, stress tolerance, and total grain weight per plant in rice. Our findings reveal insights into a unique regulatory mechanism for an on/off switch of reversible gene expression in maintaining sugar homeostatic states, which tightly regulates plant growth and development, and also highlight MYBS2 and αAmy3 as potential targets for crop improvement.

The Molecular Regulatory Pathways and Metabolic Adaptation in the Seed Germination and Early Seedling Growth of Rice in Response to Low O2 Stress

“…A recent study revealed that the transcription factor MYBS2 competes with MYBS1 for the same cis -element of the αAmy promoter and represses αAmy expression ( Figure 2 ). Via promoting or inhibiting the expression level of αAmy , the competition between MYBS1 and MYBS2 can regulate and maintain sugar within an appropriate range during germination and early seedling growth under sugar starvation stress [ 23 ].…”

“…Despite the sophisticated molecular mechanisms involved in the regulation of the anaerobic germination and seedling growth in rice, considerable progress on understanding the genetic, molecular and physiological basis of rice in response to submergence stress at the germination stage, has been achieved in the last few decades [ 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23 ]. Here, we mainly focus on reviewing the molecular genetic mechanisms that regulate the metabolic adaptation of rice to anaerobic germination stress; we could not cover all the related advances due to space limitations.…”

Evaluation of the impact of heat on wheat dormancy, late maturity α-amylase and grain size under controlled conditions in diverse germplasm

“…However, no cold shock was reported during this period 57 . In rice, accumulation of α-amylase has been described during grain developmental heat stress or more generally abiotic stress 58 . As a result, there is an emerging hypothesis that severe and rapid temperature changes may trigger LMA.…”

How does rice cope with too little oxygen during its early life?

“…Rice adh1 mutants with reduced ATP levels display decreased cell division and impaired coleoptile elongation under submergence (Takahashi et al, 2011). Both gain-and loss-offunction studies have revealed that aAmy3 is essential for submergence tolerance, but overexpression of this enzyme alone is insufficient to enhance submergence tolerance in rice seedlings (Chen et al, 2019). Higher fermentation rates, soluble carbohydrate content, and efficient energy use are important factors contributing to rice AG/ ASD abilities relative to other cereals (Mustroph et al, 2006).…”