To cope with P limitation, plants exhibit a series of physiological, biochemical, and molecular strategies such as modifying the architecture of the roots [26, 27], secreting carboxylates and acid phosphatase , elevating transcription of genes essential for P acquisition , and enhancing the remobilization of the previously stored P [19, 23, 30]. Recently, accumulating evidence has supported the participation of TFs in Pi starvation signaling , although much remains to achieve a full understanding of the Pi starvation signaling network, as well as its crosstalk with other pathways such as phytohormone signaling cascades. Furthermore, recent studies have reported that P stored in root cell wall can be reutilized in Arabidopsis and rice, and numerous phytohormones or signal molecules such as ethylene and nitric oxide (NO) participate in this process . In this study, we for the first time reported that a MYB TF is involved in the tolerance to P deficiency in A. thaliana, and found that the sensitivity of P deficiency in the loss function mutant, myb103, also showed a clear association with the cell wall, and in particular the phytohormone ethylene.
Numerous MYB TFs were reported to be involved in plant responses to environmental stresses [32, 33]. For example, HOS10 , MYB14 and MYB15 , and MdMYB23  are involved in the modulation of cold stress response while MYB12is involved in response to nitrogen deficiency . PSR1  and PHR1  are two well characterized R2R3 MYB transcription factors that have been implicated in the positive regulation of Pi stress responses. Furthermore, MYB62 has been implicated to act as a negative regulator of P starvation response , as its expression was significantly induced during P deficiency , and MYB62 overexpressing lines exhibited phosphate accumulation in roots. Moreover, MYB62 also serves as a repressor of GA biosynthesis . However, little is known about whether other MYB TFs take part in the P deficiency signaling. In the present study, we found that MYB103, a R2R3 MYB TF, was involved in the P deficiency response in Arabidopsis. The expression of MYB103 was induced under the P deficient condition in Arabidopsis (Fig. 1), and the Arabidopsis loss function mutant of MYB103 exhibited the P deficiency-sensitive phenotype (Fig. 2), with lower levels of shoot and root soluble P (Fig. 3).
Cell wall, which consists of cellulose, hemicelluloses, pectin and other matrix polysaccharides, acts as an important P repository in rice and Arabidopsis [19, 23, 40]. Among them, only pectin was demonstrated to be involved in the P recycling under the P deficient condition, as the carboxyl-acid groups in the cell wall pectin have strong affinity for cations, such as Fe3+, which lead to the release of the P [23, 41]. Our results establish the role of the P pool in cell wall pectin in WT under P deficiency, as loss function of MYB103 results in the significantly decreased P reutilization when under -P compared with +P (Fig. 5A and 5C), in company with the greatly reduced pectin content (Fig. 6B). As a result, when in comparison to WT, more P was retained in the myb103 cell wall under the -P condition (Fig. 5), thus less soluble P was found in myb103 roots and shoots, which rendered it more sensitive to the P deficiency (Figs. 2 and 3). In agreement with this, the expression of Pdeficiency-responsive genesincluding PHR1, PHT1, PHO1 and PHO2 was higher in myb103 roots than in WT under P starvation (Fig. 4).
Then, how does MYB103 regulate the cell wall P reutilization? What are the downstream signals? As we know, ethylene acts as a signal molecule that not only plays important roles in various physiological processes and plant growth, but also participates in the regulation of responses to different abiotic stresses [15, 42, 43]. While the involvement of ethylene in response to P deficiency in plants has been documented [19, 20, 44, 45], the mechanism underlying the regulation of ethylene production remains largely elusive. In the present study, we found that less ethylene was produced in roots of myb103, when compared with WT, irrespectively of the P status (Fig. 7), indicating that ethylene production is regulated by MYB103 in response to P deficient in Arabidopsis roots.
In conclusion, our results demonstrate that a R2R3 MYB TF, MYB103, is involved in the cell wall-based P reutilization under P deficiency through regulating ethylene production. Our study, thus, not only demonstrated that a single TF could be responsible for P remobilization and phytohormone-induced reutilization of cell wall P, but also provided an entry point for dissecting the association between nutritional cues and phytohormone signaling pathways.