Smart role of plant 14-3-3 proteins in response to phosphate deficiency

Abstract

Higher plants adapt to phosphorus deficiency through a complex of biological processes. Among of them, two adaptive processes are very important for the response of higher plants to phosphorus deficiency. One is the enhancement of root growth by regulating carbohydrate metabolism and allocation, and the other is rhizosphere acidification to acquire phosphorus efficiently from soil. TFT6 and TFT7, two different members of tomato 14-3-3 gene family, play the distinct roles in the adaption of plants to phosphorus deficiency by taking part in the two processes respectively. TFT6 which acts mainly in leaves is involved in the systemic response to phosphorus deficiency by regulating leaf carbon allocation and increasing phloem sucrose transport to promote root growth, while TFT7 directly functions in root by activating root plasma membrane H⁺-ATPase to release more protons under phosphorus deficiency. Based on these results, we propose that 14-3-3 proteins play the smart role in response to phosphorus deficiency in higher plants.

Plant 14–3-3 Proteins

Plant 14–3-3 proteins are phosphoserine-binding proteins that regulate the activities of a wide array of targets via direct protein-protein interactions. Higher plants have more than one 14–3-3 isoform.¹ For example, in Arabidopsis and tomato, 13 and 12 isoforms have been found respectively. In higher plants, 14–3-3 proteins possess a highly conserved target-binding domain, which is able to recognize several short consensus amino acid sequence motifs containing phosphoserine or phosphothreonine. However, data that suggest that individual 14–3-3 isoforms do have specific function in higher plants are accumulating in the literatures. First, although the 14–3-3 protein sequences are highly conserved, variation does exist within the N- and C-terminal domains. It was suggested that the N and C termini have functions in isoform specificity.² Second, there is increasing evidence that the promoter is associated with gene-specific expression patterns in higher plants. In potato, the specificity of 14–3-3 gene expression in response to stress is promoter-dependent.³ Third, in higher plants, tissue- and cell-specific expression was observed in the 14–3-3 gene family. For example, in Arabidopsis thaliana, 14–3-3 gene expression exhibited cell- and tissue-specific localization.⁴ By using real-time RT-PCR, we also find that isoform-specificity may exist in the 14–3-3 gene family of young tomato roots.⁵ However, genetic evidence is little about the plant 14–3-3 proteins isoform-specificity.

Adaption of 14–3-3 Proteins to Phosphate Deficiency

The plastic and adaptive responses by root have been proposed as the major mechanism by which plants cope with the fluctuating environments.⁶ Although phosphorus content in soil may be high, phosphorus deficiency can arise in soils due to mineralization and fixation processes. To survive, plants have developed flexible adaption to cope with soil phosphorus deficiency.⁷ These adaption include not only the increase in root length by regulating carbohydrate metabolism and allocation, but also the rhizosphere acidification to acquire phosphorus efficiently. In higher plants, 14–3-3 proteins bind to a range of transcription factors and other signaling proteins, and play roles in regulating plant development and stress responses.^8,9 Further, using transgenic Arabidopsis plants, SIET (scanning ion-selective electrode technique) and grafting technique, we found that TFT6 (one member of non-ε group in tomato 14–3-3 family) is the later responsive gene, and TFT6 which acts mainly in leaves is involved in the systemic response to low-phosphorus-stress by regulating leaf carbon allocation and increasing phloem sucrose transport to promote root growth, while TFT7 (one member of ε-like group in tomato 14–3-3 family) is the early responsive gene and directly functions in root by activating root plasma membrane H⁺-ATPase to release more protons under low-phosphorus-stress.¹⁰ These results including genetic data indicate that different plant 14–3-3 isoforms have the distinct functions under phosphate deficiency. Thus, owe to the isoform-specificity, plant 14–3-3 proteins play the smart role in response to phosphate deficiency.

Conclusions and Perspectives

TFT6 and TFT7, two different members of tomato 14–3-3 gene family, play the distinct roles in the adaption of plants to phosphorus deficiency (Fig. 1). TFT6 is involved in the systemic adaption of plants to low phosphorus stress by regulating shoot carbon allocation (mainly happen in leaf), while TFT7 is involved in the local adaption of plants to low phosphorus stress by mediating root plasma membrane H⁺-ATPase to release proton (mainly happen in root). This finding will help to further elucidate the regulative mechanisms that control plant responses to low phosphorus deficiency. However, owing to the fact that 14–3-3 proteins have a lot of targets in higher plant, comprehensive analyses including micro-arrays for the pattern of gene expression, proteomic and pull-down studies to provide information on the accurate role of TFT6 and TFT7 in plants will help to answer many more questions that remain, especially the reasons for isoform-specificity of plant 14–3-3 proteins.

Figure 1. Distinct role of TFT6 and TFT7 in adaption of plants to low phosphorus stress. P (phosphorus), SS (starch synthase), PM ATPase (plasma membrane H⁺-ATPase).

Xu WF, Shi WM, Jia LG, Liang JS, Zhang JH. TFT6 and TFT7, two different members of tomato 14-3-3 gene family, play distinct roles in plant adaption to low phosphorus stress. Plant Cell Environ. 2012 doi: 10.1111/j.1365-3040.2012.02497.x.