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.