Suppression of Photosynthetic Gene Expression in Roots Is Required for Sustained Root Growth under Phosphate Deficiency    

Abstract

Plants cope with inorganic phosphate (Pi) deficiencies in their environment by adjusting their developmental programs and metabolic activities. For Arabidopsis (Arabidopsis thaliana), the developmental responses include the inhibition of primary root growth and the enhanced formation of lateral roots and root hairs. Pi deficiency also inhibits photosynthesis by suppressing the expression of photosynthetic genes. Early studies showed that photosynthetic gene expression was also suppressed in Pi-deficient roots, a nonphotosynthetic organ; however, the biological relevance of this phenomenon remains unknown. In this work, we characterized an Arabidopsis mutant, hypersensitive to Pi starvation7 (hps7), that is hypersensitive to Pi deficiency; the hypersensitivity includes an increased inhibition of root growth. HPS7 encodes a tyrosylprotein sulfotransferase. Accumulation of HPS7 proteins in root tips is enhanced by Pi deficiency. Comparative RNA sequencing analyses indicated that the expression of many photosynthetic genes is activated in roots of hps7. Under Pi deficiency, the expression of photosynthetic genes in hps7 is further increased, which leads to enhanced accumulation of chlorophyll, starch, and sucrose. Pi-deficient hps7 roots also produce a high level of reactive oxygen species. Previous research showed that the overexpression of GOLDEN-like (GLK) transcription factors in transgenic Arabidopsis activates photosynthesis in roots. The GLK overexpressing (GLK OX) lines also exhibit increased inhibition of root growth under Pi deficiency. The increased inhibition of root growth in hps7 and GLK OX lines by Pi deficiency was completely reversed by growing the plants in the dark. Based on these results, we propose that suppression of photosynthetic gene expression is required for sustained root growth under Pi deficiency.

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

“…Likewise, the content of SGs as phosphorous-free glycolipids that replace phospholipids is known to increase in the PM as a response to phosphate starvation (Andersson et al 2005). Among other features reminiscent of Pi limitation stress in plants, the PM fraction of NM roots showed enhanced abundances of sulfite exporter, glycerol-3-phosphate transporter, and phosphoenolpyruvate carboxylase (PEPC) (Calderon-Vazquez et al 2008;Lan et al 2012;Kang et al 2014). Increased levels of PEPC in Pi-limited plants has been linked to enhanced synthesis and excretion of organic acids that increase Pi concentration in the soil solution (reviewed in Plaxton and Tran 2011).…”

Root Architecture Responses: In Search of Phosphate

“…Isolated in the same genetic forward screen as the hps1 mutant, the hps7 mutant exhibits a hypersensitive root phenotype under Pi deficiency, but this phenotype is not reversed in high Pi (Kang et al, 2014). The HPS7 gene corresponds to tyrosylprotein sulfotransferase, a protein required for the production of active sulfated phytosulfokine with absence that has pleiotropic consequences, including altered root meristem maintenance (Komori et al, 2009;Zhou et al, 2010) and enhanced Microbe Associated Molecular Pattern-triggered seedling growth inhibition (Igarashi et al, 2012).…”

“…The HPS7 gene corresponds to tyrosylprotein sulfotransferase, a protein required for the production of active sulfated phytosulfokine with absence that has pleiotropic consequences, including altered root meristem maintenance (Komori et al, 2009;Zhou et al, 2010) and enhanced Microbe Associated Molecular Pattern-triggered seedling growth inhibition (Igarashi et al, 2012). Surprisingly, expression of many photosynthetic genes is activated in roots of hps7, and their expression is further increased in low Pi; additionally, the PR tip of hps7 accumulates chlorophyll, starch, and Suc (Kang et al, 2014). Kang et al (2014) proposed that tyrosylprotein sulfotransferase acts as a master switch in the suppression of photosynthetic gene expression in roots.…”

“…Surprisingly, expression of many photosynthetic genes is activated in roots of hps7, and their expression is further increased in low Pi; additionally, the PR tip of hps7 accumulates chlorophyll, starch, and Suc (Kang et al, 2014). Kang et al (2014) proposed that tyrosylprotein sulfotransferase acts as a master switch in the suppression of photosynthetic gene expression in roots. These findings extend the data for suc2 mutants, but the molecular origin of the root growth defect of hps7 seedlings is not yet known.…”

The regulation and plasticity of root hair patterning and morphogenesis

“…In support of this assumption, the low phosphorus insensitive 4 (lpi4) mutant shows a less pronounced decrease in hydrogen peroxide maximum in response to Pi starvation than do wild-type plants and fails to display the attenuated primary root growth that is typical of Pi-deficient plants (Chacón-López et al, 2011). Moreover, a mutant that is hypersensitive to Pi starvation (hypersensitive to Pi starvation 7, hps7) accumulates high amounts of hydrogen peroxide (Kang et al, 2014). Notably, changes in ROS distribution upon nutrient starvation appear to be nutrient specific (Shin et al, 2005).…”