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Orientation of cell division is essential for plant development as the direction of growth is determined by the direction of cell expansion and orientation of cell division. We have demonstrated that cell division orientation in vascular tissue is regulated by the interactions between a receptor kinase (PXY) expressed in dividing cells and its peptide ligand (CLE41) that is localized to adjacent phloem cells. Given that other receptor kinases have been identified as orienting the cell division plane in several developmental processes, we suggest that localized signaling from adjacent cells may be a general mechanism for defining the plane of cell division.
Throughout the life of plants, new organs are generated from meristems which contain stem cells at their center. Meristematic cells divide in regulated processes resulting in displacement of daughter cells to the periphery of the meristem where they differentiate, taking on new cell identities.1 Vascular meristems (cambium and procambium) are responsible for radial growth and are the main source of plant biomass.2 Their regulation has a come under increasing scrutiny as biomass is likely to play an increasing role in generation of renewable energy.3
Arabidopsis vascular tissue is organized into discrete collateral bundles in stems,4 whereas in hypocotyls, vasculature forms in a continuous ring, much like that of trees.5 In both cases spatially separated xylem and phloem are formed along the stem mediolateral axis and are populated with cells derived from the procambium or cambium (Fig. 1). Vascular initials displaced from the meristematic zone towards the center of the stem differentiate into xylem whereas those displaced towards the outside of the stem differentiate into phloem. This organization occurs because vascular meristematic cells are long and thin and divide periclinally down their long axis, perpendicular to the mediolateral axis. Because these are highly ordered divisions, vascular tissue is characterized by long files of cells. Until recently regulatory factors which influence the highly ordered nature of these divisions—and therefore plant vascular tissue organization were entirely unknown.
PXY encodes a receptor-like kinase (RLK)6 that is expressed in the procambium.6–8 Using in situ hybridization, we have also observed PXY expression in a continuous ring in older Arabidopsis stems (Fig. 2). Within bundles, this expression occurs in the procambium, but in the interfascicular region (between the bundles), PXY is expressed in an area where secondary (cambial) growth is likely to initiate suggesting that PXY is required prior to initiation of new vascular tissue. This expression pattern is consistent with its expression pattern just below the shoot apex, where PXY expression also appears in positions where vascular tissue is likely to initiate.8 pxy mutants are characterized by intercalation of xylem and phloem, which occurs because divisions are no longer highly oriented and consequently the xylem and phloem are not spatially separated. The cause of this defect is the inability of the plants to perceive a signal that specifies the division plane. One striking phenotype that is a feature of the disrupted vasculature in pxy mutants is that xylem vessels do not run straight and parallel as they do in wild type sections. Instead, they move in and out of the plane of section suggesting that they are curved6 (Fig. 3A and B). We now present evidence that this is indeed the case. Macerated xylem vessels from pxy mutants were curved where this is clearly not the case in wild type vessels (Fig. 3D and E). This curvature may be the direct result of the inability of the pxy mutants to correctly position the phragmaplast down center of the long axis of dividing vascular initials.
We previously suggested a mechanism for how PXY RLK's might transmit positional information to specify the division plane in procambial cells.6 This model was based on a mechanism previously described in C. elegans where positioning of a cell division in EMS cells was shown to be dependent on the MOM-2 ligand signaling from an adjacent cell to the MOM-5 receptor.9 However, to test if a similar mechanism was present in PXY signaling, it was essential to identify the ligand to the PXY receptor. We reasoned that the ligand was likely to be a member of the CLE family of peptides because PXY is closely related to CLV1,10 which binds a CLE peptide.11 We analyzed expression patterns of Arabidopsis CLE genes using publicly available microarray data and became focused on CLE41 because its expression pattern was closest to that of PXY. CLE41 was subsequently shown to be expressed in phloem cells adjacent to the PXY expression domain and to bind PXY.7 Furthermore, PXY is essential for CLE41 function.7,8 Our model was confirmed by altering the positional information conferred to PXY by localized expression of CLE41. Ectopic expression of CLE41 from the 35S promoter resulted in plants in which the phloem and xylem became intercalated, the division plane of procambial cells was altered8 and mature xylem vessels did not run parallel (Fig. 3C).
Orientation of cell division is clearly a function of plant receptor kinases as several other RLK's have been identified as being required for other highly ordered cell division processes. ACR4 is required for specification of a cell division that occurs prior to lateral root initiation,12 an asymmetric cell division in Maize stomatal mother cells is controlled by PAN1;13 and division planes in apical meristems are not always ordered in the absence of members of the SUB family.14
LRR kinase—CLE signaling has well established roles in controlling cell proliferation.15,16 It is possible that regulation of both the orientation of cell division and cell proliferation represents a more general pathway by which LRR kinase—CLE signaling functions in plants. The number of CLE genes present in plant genomes has increased with the evolution of more diverse body plans. For example, the moss species Physcomitrella patens has a single CLE gene compared to 32 in Arabidopsis and 44 in rice.17 It is tempting to speculate that as the requirement for specialist cell divisions in more complex plants has arisen, specialization of receptor ligand pairs has occurred in order to fulfill these roles.
Previously published online: www.landesbioscience.com/journals/psb/article/11665