Genetic and Genomic Evidence That Sucrose Is a Global Regulator of Plant Responses to Phosphate Starvation in Arabidopsis    

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.

Expression of Sucrose Transporter cDNAs Specifically in Companion Cells Enhances Phloem Loading and Long-Distance Transport of Sucrose but Leads to an Inhibition of Growth and the Perception of a Phosphate Limitation

“…SUT OE from the Natural AtSUC2 Promoter Causes the Same Phenotype as Expression from the CoYMV Promoter It was previously shown that constitutive OE of AtSUC2 from the Cauliflower mosaic virus 35S promoter could trigger a P limitation response (Lei et al, 2011). However, this might be due to inappropriate expression of Suc transport activity in cells that normally do not accumulate Suc from the apoplast.…”

“…Both a reduction in photosynthesis and stem girdling, which blocks phloem transport, attenuate P deficiency responses in roots, including a decrease in the expression of many PSI genes (Liu et al, 2005;Karthikeyan et al, 2007). In addition, it was recently shown that ubiquitous SUT OE can induce a P deficiency response (Lei et al, 2011), potentially by disrupting normal Suc distribution patterns. It is understandable that normal and efficient Suc transport is required for an effective response to P limitation, because P limitation induces processes that have a high demand for photoassimilate, such as growth of lateral roots and root hairs, changes in gene expression, remodeling of metabolism, secretion of organic acids, and energization of membranes (Misson et al, 2005;Morcuende et al, 2007;Plaxton and Tran, 2011;Veneklaas et al, 2012).…”

“…To test if companion cell-specific OE of SUT genes enhances PSI gene expression in the absence of exogenous Suc, representative PSI genes were analyzed by RT-qPCR. AtPT2 (PHT1;4, At2G38940) and PHT2;1 (At3G26570) are inorganic P transporters induced by P starvation (Karthikeyan et al, 2007;Lei et al, 2011). Both had higher expression levels in the SUT OE lines than in the wild type (Fig.…”

“…Conversely, utilization of sugars and storage carbohydrates requires P for metabolism, which occurs mostly by ATPdependent formation of phosphoesters. Recently, the mutation hypersensitive to phosphate starvation1 (hps1) was isolated in an activation-tagging screen as having enhanced sensitivity to P deficiency (Lei et al, 2011). Interestingly, hps1 results in ectopic and ubiquitous activation of AtSUC2, and growing hps1 mutants in the presence of excess P reversed the pleiotropic effects.…”

“…Interestingly, hps1 results in ectopic and ubiquitous activation of AtSUC2, and growing hps1 mutants in the presence of excess P reversed the pleiotropic effects. The authors argued that Suc is a global regulator of P starvation (Lei et al, 2011).…”