Mechanisms of plant root xylem developmental plasticity in response to water deficiency and salt

Abstract: Plants may be exposed to a variety of different environmental conditions including water deficiency and salt, both affecting the uptake of water into the plant. Water is taken up from the soil by the roots and distributed throughout the plant via the water conducting tissue, the xylem. Plants are remarkably plastic and have evolved different mechanisms to sense the environment and adjust their development accordingly. However, how xylem development may respond to water availability is not clear. In this thesis, I show how water deficiency and salt affect xylem development and how the observed phenotypic alterations are regulated on a molecular level. We found that upon water deficiency additional protoxylem strands were formed along with an early differentiation of the inner metaxylem. These phenotypes were regulated both by non-cell autonomous and cell autonomous signaling via the hormone abscisic acid (ABA). The expression of microRNA165 was induced by ABA signaling in the endodermis leading to downregulation of homeo domain leucine zipper class III (HD-ZIP III) transcription factors in the stele. This caused a shift in xylem identity from meta- to protoxylem and the formation of additional protoxylem strands. At the same time, cell autonomous ABA signaling upregulated several VASCULAR RELATED NAC DOMAIN (VND) transcription factors including VND7, which promoted the shift in xylem identity as well as VND2 and VND3, which promoted early differentiation of the inner metaxylem. In contrast, during an initial phase of salt stress, we observed the formation of protoxylem gaps specifically in response to ionic stress and distinct from ABA-signaling. We identified that protoxylem gaps were caused by lowered levels and signaling of the growth regulator gibberellin (GA). Downstream of GA-signaling, protoxylem gap formation upon salt was controlled by genes involved in secondary cell wall formation including the xylem master regulator VND6 and factors involved in cell wall modification. Salt tolerance assays suggested that protoxylem gaps may contribute to salt tolerance and the phenotypes that we observed upon water deficiency have been suggested to confer drought tolerance. We observed similar effects on xylem developmental plasticity in response to water deficiency and salt in various different dicot species indicating an evolutionary conservation. Thus, xylem development is of high relevance for breeding programs to generate plant varieties better adapted to a changing climate.