Stem cell function during plant vascular development

Abstract

The plant vascular system, composed of xylem and phloem, evolved to connect plant organs and transport various molecules between them. During the post-embryonic growth, these conductive tissues constitutively form from cells that are derived from a lateral meristem, commonly called procambium and cambium. Procambium/cambium contains pluripotent stem cells and provides a microenvironment that maintains the stem cell population. Because vascular plants continue to form new tissues and organs throughout their life cycle, the formation and maintenance of stem cells are crucial for plant growth and development. In this decade, there has been considerable progress in understanding the molecular control of the organization and maintenance of stem cells in vascular plants. Noticeable advance has been made in elucidating the role of transcription factors and major plant hormones in stem cell maintenance and vascular tissue differentiation. These studies suggest the shared regulatory mechanisms among various types of plant stem cell pools. In this review, we focus on two aspects of stem cell function in the vascular cambium, cell proliferation and cell differentiation.

Figure 1

Regulation of stem cells and their niches in Arabidopsis. (A–C) The organization of stem cell niche in shoot apical meristem (SAM) (A), root apical meristem (RAM) (B) and vascular cambium (C), and their WUS-CLV regulatory mechanism in each meristem. In SAM and RAM, the stem cells are adjacent to the niche cells, which maintain their pluripotency (A, B). In RAM, daughter cells of stem cells are committed into specific cell fates depending on their position (B). (D) The location of SAM and RAM is indicated in 5-day-old Arabidopsis seedling.

Figure 2

Organization of vascular tissues in Arabidopsis root and Populus stem. (A) A schematic cross-section of Arabidopsis root showing the vascular organization during the primary development. (B, C) Cross-sections of Arabidopsis root (B) and Populus stem (C) during the secondary development.

Figure 3

The initiation and formation of procambium cells is regulated by the auxin-mediated positive feedback loop. (A) Schemes of longitudinal median sections during early embryogenesis in Arabidopsis. (B) The polar localization of PIN1 and the expression pattern of MP during early Arabidopsis embryogenesis. (C) The auxin-mediated regulatory loop controlling the vascular initiation during leaf vein growth.

Figure 4

Schematic illustration of the primary and secondary stem anatomy in Arabidopsis. The primary stem exhibits disconnected vascular bundles with procambium. In the secondary developmental phase, this procambium turns into a fascicular cambium and the cells between bundles become an interfascicular cambium. Fascicular and interfascicular cambia interconnect to each other and establish a cambium in a circular form.

Figure 5

Cell type patterning in Arabidopsis roots is controlled by the bidirectional cross-talk mediated by SHR and microRNA 165/166 that are mobile between cells. SHR, generated in the stele, travels to the endodermis and activates the expression of microRNA 165/6. MicroRNA 165/6 from the endodermis travels to the vascular cylinder and degrades mRNAs of HD-ZIP III transcription factors in the endodermis and periphery of vascular cylinder, resulting in a graded distribution of HD-ZIP IIIs. A high level of HD-ZIP IIIs specifies metaxylem and a low level specifies protoxylem.

Figure 6

The regulatory loop between auxin and cytokinin controls vascular patterning in the Arabidopsis primary root. Cytokinin signalling restricts the auxin signalling maximum to the xylem axis by promoting the bisymmetric localization of PINs. Consequently, auxin activates the expression of AHP6 in the protoxylem position, and in turn AHP6 counteracts cytokinin signalling, thereby allowing cells to differentiate into protoxylem.

Figure 7

Hormonal regulation in the vascular stem cells.

Figure 8

Regulatory networks in the control of vascular stem cell activities.