Genetic and genomic evidence that sucrose is a global regulator of plant responses to phosphate starvation in Arabidopsis.

Mingguang Lei,Dong Liu,Yingtao Zhao,Kashchandra G Raghothama,Baocai Zhang,Yidan Liu,Xiujie Wang,Yihua Zhou

doi:10.1104/pp.110.171736

Abstract

Plants respond to phosphate (Pi) starvation by exhibiting a suite of developmental, biochemical, and physiological changes to cope with this nutritional stress. To understand the molecular mechanism underlying these responses, we isolated an Arabidopsis (Arabidopsis thaliana) mutant, hypersensitive to phosphate starvation1 (hps1), which has enhanced sensitivity in almost all aspects of plant responses to Pi starvation. Molecular and genetic analyses indicated that the mutant phenotype is caused by overexpression of the SUCROSE TRANSPORTER2 (SUC2) gene. As a consequence, hps1 has a high level of sucrose (Suc) in both its shoot and root tissues. Overexpression of SUC2 or its closely related family members SUC1 and SUC5 in wild-type plants recapitulates the phenotype of hps1. In contrast, the disruption of SUC2 functions greatly inhibits plant responses to Pi starvation. Microarray analysis further indicated that 73% of the genes that are induced by Pi starvation in wild-type plants can be induced by elevated levels of Suc in hps1 mutants, even when they are grown under Pi-sufficient conditions. These genes include several important Pi signaling components and those that are directly involved in Pi transport, mobilization, and distribution between shoot and root. Interestingly, Suc and low-Pi signals appear to interact with each other both synergistically and antagonistically in regulating gene expression. Our genetic and genomic studies provide compelling evidence that Suc is a global regulator of plant responses to Pi starvation. This finding will help to further elucidate the signaling mechanism that controls plant responses to this particular nutritional stress.

Highlights

Protein Science Laboratory of the Ministry of Education, School of Life Sciences, Tsinghua University, Beijing 100084, China (M.L., Y.L., D.L.); State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology (B.Z., Y.Zho.), and State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology (Y.Zha., X.W.), Chinese Academy of Sciences, Beijing 100101, China; and Department of 2Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (K.G.R.)
To confirm that the enhanced expression of AtPT2-LUC was due to the mutation that occurred in a regulatory component, an AtPT2-GUS marker gene was introduced into hps1 plants through a genetic cross
This work defines a broader role for Suc in many of the observed Pi starvation responses in Arabidopsis and tries to explore how Suc acts at the molecular level in regulating these responses through genetic and genomic analyses of a Suc overaccumulation mutant, hps1

Summary

Introduction

Through the long evolution process, plants have developed sophisticated strategies to better adapt to Pi starvation (Yuan and Liu, 2008) These strategies include changes in the root architecture system (i.e. reduction of primary root growth and the formation of more lateral roots and root hairs), increased expression of Pi transporter genes, the induction and secretion of organic acid, RNase, and acid phosphatases (APases), and the accumulation of starch and anthocyanin. These adaptive responses have been widely studied and well documented in a variety of plant species, the molecular mechanisms that regulate these responses are still largely unknown. Other transcription factors that are involved in Pi responses include WRKY75, WRKY6, ZAT6, MYB26, and BHLH32 in Arabidopsis (Arabidopsis thaliana) and

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