Sucrose nonfermenting-1-related protein kinase 1 regulates sheath-to-panicle transport of nonstructural carbohydrates during rice grain filling

Abstract

The remobilization of non-structural carbohydrates (NSCs) reserved in rice (Oryza sativa) sheaths is essential for grain filling. This assimilate distribution between plant tissues and organs is determined by sucrose non-fermenting-1-related protein kinase 1 (SnRK1). However, the SnRK1-mediated mechanism regulating the sheath-to-panicle transport of NSCs in rice remains unknown. In this study, leaf cutting treatment was used to accelerate NSC transport in the rice sheaths. Accelerated NSC transport was accompanied by increased levels of OsSnRK1a mRNA expression, SnRK1a protein expression, catalytic subunit phosphorylation of SnRK1, and SnRK1 activity, indicating that SnRK1 activity plays an important role in sheath NSC transport. We also discovered that trehalose-6-phosphate, a signal of sucrose availability, slightly reduced SnRK1 activity in vitro. Since SnRK1 activity is mostly regulated by OsSnRK1a transcription in response to low sucrose content, we constructed an snrk1a mutant to verify the function of SnRK1 in NSC transport. NSCs accumulated in the sheaths of snrk1a mutant plants and resulted in a low seed setting rate and grain weight, verifying that SnRK1 activity is essential for NSC remobilization. Using phosphoproteomics and parallel reaction monitoring, we identified 20 SnRK1-dependent phosphosites that are involved in NSC transport. In addition, the SnRK1-mediated phosphorylation of the phosphosites directly affected starch degradation, sucrose metabolism, phloem transport, sugar transport across the tonoplast, and glycolysis in rice sheaths to promote NSC transport. Therefore, our findings reveal the importance, function, and possible regulatory mechanism of SnRK1 in the sheath-to-panicle transport of NSCs in rice.

Targeting TOR and SnRK1 Genes in Rice with CRISPR/Cas9

“…Hence, snrk1αa mutants were compromised in yield components as compared to the WT. These results corroborate recent reports of reduced plant height and reduced seed set in Os SnRK1αA knock-out plants grown in normal conditions [ 20 , 33 ].…”

“…Lu et al [ 37 ] isolated T-DNA insertion lines of rice SnRK1αA_ LOC_Os05g45420 and SnRK1αC_ LOC_Os08g37800 and found that germination and seedling growth are impacted in snrk1αa but not in snrk1αc mutant. More recently, rice mutants in SnRK1αA were developed by CRISPR/Cas9 that were instrumental in deciphering the regulation of sugar homeostasis under normal conditions or starvation and translocation of starch from sheath to panicle during grain filling in rice [ 20 , 33 ]. However, this is the first time, to our knowledge, snrk1αb + snrk1αc double-mutants are reported.…”

Sugar transport from sheaths to seeds: A role for the kinase SnRK1

“…Taken together, the phenotypical and biochemical analyses presented in Hu et al (2022) offer insights in the process of grain filling in rice. SnRK1, an essential kinase for plant development and growth, was shown to play a critical role in NSC remobilization from sheaths to grain.…”

“…In the current issue of Plant Physiology , Hu et al (2022) present a study on NSC remobilization during grain filling in Nipponbare, a rice cultivar with a sequenced genome. Using a detailed time-course analysis to measure multiple physiological and biochemical parameters during the period following anthesis, Hu et al found that the sheath is a major source of NSC for grain filling.…”

How to switch on a master switch

“…It phosphorylates and inactivates key metabolic enzymes, such as HMG-CoA reductase, nitrate reductase, and sucrose phosphate synthase ( Sugden et al ., 1999 ), and is involved in regulating the expression of genes encoding α-amylase ( Laurie et al ., 2003 ; Lu et al ., 2007 ) and asparagine synthetase ( Baena-González et al ., 2007 ). The authors have previously shown SnRK1 to be required for the remobilization of non-structural carbohydrates in rice sheaths during grain filling ( Hu et al ., 2022 ), and it is also involved in the re-allocation of carbon in response to herbivory ( Schwachtje et al ., 2006 ). SnRK1 also promotes starch accumulation in grains and tubers through modulation of sucrose synthase and ADP-glucose pyrophosphorylase gene expression ( Kanegae et al ., 2005 ; McKibbin et al ., 2006 ) and ADP-glucose pyrophosphorylase redox activation ( Tiessen et al ., 2003 ).…”