The Plant Vascular System: Evolution, Development and FunctionsF

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Insights into Plant Vascular Biology 303 Figure 6. Vascular patterning is regulated by KANADI and Class III HD-ZIP genes and the phytohormones auxin and cytokinin. (A) In shoot vascular bundles, the default radial pattern has phloem located abaxially and xylem adaxially. (B) In the phb phv rev mutant, phloem surrounds xylem. (C) Conversely, in Class III HD-ZIP gain-of-function mutants and kan1 kan2 kan3, xylem surrounds phloem. (D) Class III HD-ZIP genes are regulated by miR165/166 and interact with auxin and brassinosteroids. (E) In the root, auxin is restricted to the xylem axis by the presence of cytokinin. (F) In mutants with defective cytokinin signaling such as wol, auxin is abundant throughout the stele, leading to ubiquitous protoxylem differentiation and loss of phloem identity. xylem axis), phloem identity is not observable directly above the QC. The first newly formed cell walls associated with phloem development are only visible 27 µm above the QC. At a distance of 69 µm, the first protophloem SEs are clearly present. Hormonal balance determines the development of vascular poles in the root Cytokinin, an essential phytohormone for development in the root, is required for vascular patterning and the differentiation of all cell types except the protoxylem. Recently, it has been shown that the root vascular pattern is defined by a mutually inhibitory interaction between cytokinin and auxin (Bishopp et al. 2011a, 2011b). If cytokinin signaling is disturbed, as in the WOODEN LEG mutant, wol or the triple cytokinin receptor mutant ahk2 ahk3 ahk4 (ARABIDOPSIS HISTIDINE KINASE), or if cytokinin levels are reduced, as is found in transgenic plants overexpressing CYTOKININ OXIDASE, the effect is always an increased number of protoxylem cell files and the loss of other cell types in the root vasculature. The domain of cytokinin activity is restricted by the action of the cytokinin signaling inhibitor, ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN 6 (AHP6). Only through this mechanism does protoxylem differentiation occur in a spatially specific manner, allowing for the proper development of the phloem cell types.
304 Journal of Integrative Plant Biology Vol. 55 No. 4 2013 Phloem differentiation Sieve elements comprise the main conductive tissue of the phloem. Like the CCs, they originate from phloem precursor cells in the procambium. However, very early in primary phloem development, they undergo dramatic changes in their morphology. As the SEs mature, they experience extensive degradation of their organelles. The nucleus, vacuoles, rough endoplasmic reticulum (ER) and Golgi are degraded in a process which has not yet been characterized at the molecular level. This reduction in cellular contents establishes an effective transport route through the sieve tubes. However, the SEs still remain living, as they retain a plasma membrane and a reduced number of other organelles, such as smooth ER, plastids and mitochondria. The residual ER is localized near the PD which interconnect the SEs to their neighboring CCs. The cell walls of the SEs also undergo drastic changes in structure. The first observable process is an increase in callose that is deposited in platelet form around the PD of the SEs, replacing the already present cellulose. The cell walls which form the interface to adjoining SEs contain a high density of these callose-ensheathed PD. As these SEs mature, both these callose deposits and the middle lamella in these regions of the cell wall are removed, thereby forming a sieve plate with enlarged pores (Lucas et al. 1993). The lateral cell walls of SEs also develop specialized areas of PD-derived pores, which are called lateral sieve areas. Recent studies have shown that CALS3 and CALS7 are involved in depositing PDcallose during this developmental process (Vatén et al. 2011; Xie et al. 2011). The newly formed sieve plates, in combination with the lateral sieve areas, enable each individual SE to become a component of an integrated sieve tube system that can facilitate effective fluid transport by bulk flow. It is also noteworthy that these pores increase considerably in size as tissues age, thus increasing the transport potential of the more mature vasculature (Truernit et al. 2008). The survival and differentiation of SEs depends on a close association with their neighboring CCs, a specialized type of parenchyma cell. The cytoplasm of the CC is unusually dense, due in part to an increased number of plastids, mitochondria and free ribosomes (Cronshaw 1981). The CCs are connected to their adjacent SEs by numerous branched PD. Through these connections, the enucleate SEs are supplied with energy, assimilates and macromolecular compounds, such as proteins and RNA (Raven 1991; Lough and Lucas 2006). The size exclusion limit of these PD connections usually lies between 10 and 40 kDa (Kempers and van Bel 1997), giving credence to the concept of protein transport from CCs to SEs. The morphological and physiological uniqueness of the phloem cell types described above is also a result of specific gene expression patterns, as shown by recent transcriptome studies (Lee et al. 2006; Brady et al. 2007, 2011). These transcriptional programs are exquisitely controlled in space and time. To understand how these unique cell identities are acquired, a deeper understanding of these programs is absolutely essential. Microarray analyses of a high-resolution set of developmental time points, and a comprehensive set of cell types within the root, has resulted in the most detailed root expression map to date. Numerous distinct expression patterns have been identified through these analyses, several of which are specific to SEs or to SEs and CCs together. More than a thousand genes have been identified as having phloem-specific expression, highlighting the phloem as a highly specialized tissue within the stele. The data from these microarray studies has been made publicly available in the AREX LITE: The Arabidopsis Gene Expression Database (arexdb.org), providing an invaluable resource for future studies on phloem function. Bauby et al. (2007) identified several phloem markers, which they named Phloem Differentiation 1–5 (PD1-PD5) by screening the Versailles collection of gene trap mutants for plant lines expressing the uidA reporter gene in immature vascular tissues. PD1-4 were restricted to protophloem cells, as determined by their cell shape. However, PD5 was expressed in both protophloem and metaphloem cells. Using these markers, these authors could track the onset of phloem development directly after embryogenesis. PD4 is expressed in the tips of leaf primordia some 3 days after germination (dag). Spreading from there, by 7 dag, PD4 has already traced out the entire future leaf vasculature. The first expression of PD1 and PD3 was detected 3 dag in the proximal protophloem of leaf primordia. These results establish that PD1 and PD3 are expressed during the differentiation of protophloem. PD4 and PD5 gene reporter-based expression was also detected in the location of the midveins and higher order veins before procambium differentiation, thereby defining the pre-patterning of the future veins. Regulation of phloem differentiation Currently, only two factors are known which specify phloem identity: ALTERED PHLOEM DEVELOPMENT (APL) and OC- TOPUS (OPS). APL is a MYB coiled-coil transcription factor essential for the proper differentiation of both SEs and CCs (Bonke et al. 2003). Additionally, APL contributes to the spatial limiting of xylem differentiation, is expressed both in SEs and CCs, and has been shown to be nuclear localized. Loss of APL function has an extraordinary effect on the phloem, as can be observed in the loss-of-function mutant apl1 (Figure 7). This mutant is seedling-lethal and results in short-rooted plants. Neither CCs nor SEs can be detected in cross-sections of apl1 plants. Furthermore, phloem-specific reporters, such as the CC-specific sucrose transporter, SUC2, or the proto SE reporter, J0701, cease to be expressed entirely in these mutant
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The Plant Vascular System: Evolution, Development and FunctionsF

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