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 photoassimilates 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 re-shapes the process, which molecular mechanisms link environmental inputs with developmental outputs, which gene regulatory networks facilitate the genetic adaptation of vascular development to environmental niches, or how the first vascular cells appeared as an evolutionary innovation. In this review, we (1) summarize the current knowledge of the mechanisms involved in vascular development, focusing on the model species Arabidopsis thaliana, (2) describe the anatomical effect of specific environmental factors on the process, (3) speculate about the main entry points through which the molecular mechanisms controlling of the process might be altered by specific environmental factors, and (4) discuss future research which could identify the genetic factors underlying phenotypic plasticity of vascular development.

Keywords: Cambium; Phloem; Plasticity; Wood; Xylem.

Fig. 1

Organization of plant vascular tissues. a Appearance of the provascular tissue at the end of embryo development. b Localization of the procambial, phloem and xylem tissues within primary vasculature in veins and in the root of young seedlings. c Secondary growth in stems. In Arabidopsis (and other dicotyledonous plants), primary vasculature appears in bundles with the phloem facing outwards and the xylem inwards, separated by a layer of procambial cells. Secondary growth requires the sequential formation of a cambial ring between bundles and the stimulation of periclinal cell divisions. d Secondary growth in roots also involves expansion of xylem at the expense of the cambium

Fig. 2

Mechanism for provascular specification during embryo development. a Illustration of the localization of (1) the initial cells in the globular-stage embryo from which all vascular tissues originate and (2) the periclinal divisions that give rise to additional vascular cells in a heart-stage embryo. b Gene regulatory network that determines vascular cell identity and cell divisions during embryo development. In response to local accumulation of auxin, the MP auxin-dependent transcription factor enhances auxin accumulation through the upregulation of the PIN1 auxin transporter, establishes vascular identity by inducing the ATHB8 HD-ZIP III transcription factor, and promotes periclinal cell divisions via TMO5-LHW-mediated increase in CK synthesis

Fig. 3

Mechanism for xylem specification and maintenance in the primary root. a Tissue layer organization surrounding the vascular cylinder of the primary root. The xylem axis in the center is surrounded by vascular-competent stem cells (procambium) and with two phloem poles on opposite ends. b Gene regulatory network that coordinates CK-dependent cell proliferation in the procambium, with auxin-mediated xylem cell-type specification. Xylem specification depends on high local auxin signaling via MP and is also achieved by high HD-ZIP III localization in the xylem precursor cells. MP activity is not only responsible for the attenuation of CK signaling in xylem precursor cells, but also for triggering the ACL5-dependent inhibitory loop that maintains appropriate levels of the LHW–TMO5 complex

Fig. 4

Cell differentiation pathways which produce the diverse phloem and xylem cell types. Illustration of the formation of different phloem and xylem cell types from unique vascular stem cells. Xylem cells include the dead vessels (tracheary elements) and fiber cells with extensive secondary cell wall deposition, along with live xylem parenchyma cells. Phloem is composed of the sieve elements and the phloem companion cells. Pink circles depict cell nuclei, and white ellipses are vacuoles

Fig. 5

Gene regulatory network for the differentiation of xylem fibers and the two types of vessels. The different cell identities are established by specific expression of VND6 (metaxylem, MX), VND7 (protoxylem, PX), and SND1/NST3 (fibers) transcription factors. SCW synthesis is regulated by the second tier of MYB transcription factors, while programmed cell death is regulated by the ACL5 thermospermine synthase. Additionally, fiber formation is absolutely dependent on STM and KNAT1 activity and this is stimulated by low DELLA levels achieved by high GA production, which is thought to be regulated by receptor-like kinases such as ER and ERL1

Fig. 6

Regulatory mechanism of cambial activity and secondary growth. a Scheme of stem vascular bundles showing the bifacial cambium. b Gene regulatory network coordinates cambial cell proliferation and the production of phloem and xylem on opposite sides of the cambium. This organization is the result of several regulatory interactions: (1) the PXY receptor-like kinase is activated by the phloem-generated TDIF signal (CLE41, 42, 44 peptides) and induces the WOX transcription factors which, in turn, promote cell proliferation in the cambium; (2) auxin modulates cell proliferation with opposing effects that involve the attenuation of CK signaling and the upregulation of WOX genes; (3) xylem specification is promoted by the PXY-dependent repression of brassinosteroid signaling and by the positive effect of auxin on HD-ZIP III expression in xylem precursor cells; (4) phloem is regulated by the mobile PEAR transcription factors that are upregulated by CK in the cambium

Fig. 7

Possible mechanisms for environmental regulation of vascular development. Three processes have been reported to be under environmental control: (1) cell proliferation in the cambium, which is inhibited by drought via the reduction in root-to-shoot CK transport, and stimulated by mechanical stress via auxin upregulation; (2) proliferation of xylem cells to increase water transport potential or counteract possible consequences of vessel cavitation; this is activated by drought through the ABA-dependent upregulation of miR165 (allowing for the reduction in HD-ZIP III activity), and also by mechanical stress in an auxin-dependent manner and (3) the production of secondary cell wall components, which is increased by drought and salt through the upregulation of specific cell wall enzymes; moreover, the relative composition of SCW material is also modulated by mechanical stress (with an increase in fiber cell production) and by temperature (which affects the activity of ESK, an enzyme that modifies xylan)