Plant vascular development: mechanisms and environmental regulation

Abstract

Plant vascular development is a complex process culminating in the generation of xylem and phloem, the plant transporting conduits. Xylem and phloem arise from specialized stem cells collectively termed (pro)cambium. Once developed, xylem transports mainly water and mineral nutrients and phloem transports photo-assimilates and signaling molecules. In the past few years, major advances have been made to characterize the molecular, genetic and physiological aspects that govern vascular development. However, less is known about how the environment reshapes the process, which molecular mechanisms link environmental inputs with developmental outputs, which gene regulatory networks facilitated the genetic adaptation of vascular development to environmental niches, or how the first vascular cells appeared as an evolutionary innovation. In this review, we (i) summarize the current knowledge of the mechanisms involved in vascular development, focusing on the model species Arabidopsis thaliana, (ii) describe the anatomical effect of specific environmental factors on the process, (iii) speculate about the main entry points through which the molecular mechanisms controlling of the process might be altered by specific environmental factors, and (iv) discuss future research which could identify the genetic factors underlying phenotypic plasticity of vascular development. Response to Reviewers: Thanks for the reviewer's comments. We have introduced all the minor changes/corrections suggested, although we have not highlighted them in the text version that we submit here. In fact, the manuscript has been extensively edited for language issues by a native speaker (acknowledged at the end of the text), shortening the sentences and writing with a more direct style. Of course, we have made sure that the message has not been altered at all.

How roots and shoots communicate through stressful times

“…Recently, the emergence of single-cell sequencing technology enables the identification of cells at intermediate differentiation states and facilitates exploration of the ontogeny of different vasculature cell types [98][99][100][101], which will help us to understand the developmental plasticity of these vascular transport vessels. Intriguingly, many regulatory pathways or key growth regulators in the vascular system have now been shown to control growth plasticity and were demonstrated to be responsive to environmental challenges (Figure 2C) [67,93]. Further investigations of how these key regulators and pathways coordinate growth and stress response will improve our knowledge on the interorgan communications that benefit plants as a whole.…”

“…Root vasculature specification and patterning events occur early during embryogenesis. Subsequent post-embryonic development and maintenance of root vasculature is a complex process that occurs in the root apical meristem (Box 1; reviewed in [67]). Root vascular architecture is highly flexible in response to environmental stresses.…”

“…Auxin and cytokinin (CK) signaling play central roles in regulating vasculature development, and are also the two main mobile hormones transported via the vascular system. During embryo development, cotyledon-derived auxin is transported to the embryonic root to form a feedback loop with CK that maintains vasculature development (reviewed in [67]). The auxin response transcription factor MONOPTEROS/AUXIN RESPONSE FACTOR 5 (MP/ARF5) regulates the downstream basic helix-loop-helix (bHLH) transcription factors TARGET OF MONOPTEROSs (TMOs) including TMO3, TMO5, and TMO6 to control the early cell division events of the provascular cells [67].…”

“…During embryo development, cotyledon-derived auxin is transported to the embryonic root to form a feedback loop with CK that maintains vasculature development (reviewed in [67]). The auxin response transcription factor MONOPTEROS/AUXIN RESPONSE FACTOR 5 (MP/ARF5) regulates the downstream basic helix-loop-helix (bHLH) transcription factors TARGET OF MONOPTEROSs (TMOs) including TMO3, TMO5, and TMO6 to control the early cell division events of the provascular cells [67]. TMO5 dimerizes with LONESOME HIGHWAY (LHW) to activate the expression of CK biosynthesis genes LOG3 and LOG4 which regulate periclinal cell divisions in (pro)cambium for secondary growth to produce new vasculature tissues [102].…”

Wood Formation under Severe Drought Invokes Adjustment of the Hormonal and Transcriptional Landscape in Poplar

“…A further consequence of drought stress is the acclimation of the xylem architecture [ 8 ]. In angiosperms, the xylem is composed of vessels, fibers, and parenchyma cells.…”