Final Report Summary - SIDEWAYS (Final size determination through spatio-temporal regulation of phytohormone signaling pathways)
A fundamental question in developmental biology relates to the mode through which the final size of a cell, organ, and whole organism is set. Plant growth involves consecutive stages of cell proliferation and post-mitotic cell enlargement. In roots, these stages form a developmental gradient along the apical–basal axis that ultimately determines their length. Small molecule hormone signaling pathways lie at the heart of this growth control. Despite dramatic advances in identifying signalling components, understanding of their spatiotemporal activities and how they integrate to coordinate whole-organ growth is just beginning to take form. Our long term goal is to understand how hormones, with the focus on the plant steroid hormones brassinosteroids (BRs), regulate growth and development. In particular we are interested in analysing the spatio-temporal regulation of the BR pathway, understanding to what extent cell-cell communication is involved during growth of and investigate how mechanical signals integrate with hormonal mediated growth control. In this grant we asked the following main questions: What is the spatio-temporal regulation of BR signal transduction and to what extent cell-cell communication is involved? What is the molecular basis for cell-cell communication? and How mechanical and phytohormone signals integrate to control final size?
Using the Arabidopsis primary root as a model organ, we initially characterized the role of BRs in the root meristem. We showed that BRs are required to maintain normal cell cycle activity and cell expansion. These two processes ensure the coherent gradient of cell progression, from the apical to the basal meristem. We further demonstrated that BR signaling in the root epidermis and not in the inner tissues is sufficient to control root meristem. Next, we investigated the elusive nature of the non-autonomous signal from the epidermis and the role of BR signaling in the inner tissues. Strikingly, we found that BR signal coordinates root growth by evoking distinct and often opposing responses in specific tissues. Whereas epidermal BR signal promotes stem cell daughter proliferation, the stele-derived BR signal induces their differentiation. Using a comprehensive tissue-specific translatome survey, we uncovered a context-specific effect of BR signaling on gene expression. Auxin genes, activated by epidermal BR perception, are necessary for induction of cell division. Conversely, the stele BR perception, accompanied by gene repression, restrains the epidermal effect. Therefore, a site-specific BR signal is essential for balanced organ growth (Fig. 1, left pane;).
In parallel, we found that coordination between two types of epidermal root cells, hair and nonhair cells, establishes root sensitivity to BR. While expression of the BR receptor BRI1 in hair cells promotes cell elongation in all tissues, its high relative expression in nonhair cells is inhibitory. These results show that the relative spatial distribution of BRI1, and not its absolute level, fine-tunes growth We showed that elevated ethylene and local cell wall modification by deposition of crystalline cellulose underlie the inhibitory effect of BRI1. We speculate that mechanisms coordinating BR signaling between hair and nonhair cells, and thereby whole root growth, involve interwoven genetic and mechanical factors.
BR research is of special agriculture interest since BR application and BR genetic modification have been shown to significantly increase crop yield and to play an important role in plant thermotolerance. Hence, the high-resolution and precise knowledge of BR function and its genomic targets established by my team is also valuable for improving crop traits without unwanted impairment of unrelated pathways.
The aforementioned achievements were a direct result of the CIG grant. The CIG grant contributed tremendously to my ability to assemble an excellent and highly motivated research team, to win competitive grants and publish high profile scientific papers. In addition, it enabled my team to integrate into the Israeli/European scientific community, implicated in invitation to international meetings in Europe and joint collaborations with different labs. Our research has gained attention by highlights in Faculty1000 and by two prestigious prizes from the Technion, one to myself and another to my graduate student. Taken together, this grant made a significant impact on my prospects to receive full tenure and subsequently a position as Full Professor.
Using the Arabidopsis primary root as a model organ, we initially characterized the role of BRs in the root meristem. We showed that BRs are required to maintain normal cell cycle activity and cell expansion. These two processes ensure the coherent gradient of cell progression, from the apical to the basal meristem. We further demonstrated that BR signaling in the root epidermis and not in the inner tissues is sufficient to control root meristem. Next, we investigated the elusive nature of the non-autonomous signal from the epidermis and the role of BR signaling in the inner tissues. Strikingly, we found that BR signal coordinates root growth by evoking distinct and often opposing responses in specific tissues. Whereas epidermal BR signal promotes stem cell daughter proliferation, the stele-derived BR signal induces their differentiation. Using a comprehensive tissue-specific translatome survey, we uncovered a context-specific effect of BR signaling on gene expression. Auxin genes, activated by epidermal BR perception, are necessary for induction of cell division. Conversely, the stele BR perception, accompanied by gene repression, restrains the epidermal effect. Therefore, a site-specific BR signal is essential for balanced organ growth (Fig. 1, left pane;).
In parallel, we found that coordination between two types of epidermal root cells, hair and nonhair cells, establishes root sensitivity to BR. While expression of the BR receptor BRI1 in hair cells promotes cell elongation in all tissues, its high relative expression in nonhair cells is inhibitory. These results show that the relative spatial distribution of BRI1, and not its absolute level, fine-tunes growth We showed that elevated ethylene and local cell wall modification by deposition of crystalline cellulose underlie the inhibitory effect of BRI1. We speculate that mechanisms coordinating BR signaling between hair and nonhair cells, and thereby whole root growth, involve interwoven genetic and mechanical factors.
BR research is of special agriculture interest since BR application and BR genetic modification have been shown to significantly increase crop yield and to play an important role in plant thermotolerance. Hence, the high-resolution and precise knowledge of BR function and its genomic targets established by my team is also valuable for improving crop traits without unwanted impairment of unrelated pathways.
The aforementioned achievements were a direct result of the CIG grant. The CIG grant contributed tremendously to my ability to assemble an excellent and highly motivated research team, to win competitive grants and publish high profile scientific papers. In addition, it enabled my team to integrate into the Israeli/European scientific community, implicated in invitation to international meetings in Europe and joint collaborations with different labs. Our research has gained attention by highlights in Faculty1000 and by two prestigious prizes from the Technion, one to myself and another to my graduate student. Taken together, this grant made a significant impact on my prospects to receive full tenure and subsequently a position as Full Professor.
