Plant Development: PXY and Polar Cell Division in the Procambium
2007; Elsevier BV; Volume: 17; Issue: 15 Linguagem: Inglês
10.1016/j.cub.2007.05.066
ISSN1879-0445
Autores Tópico(s)Plant nutrient uptake and metabolism
ResumoThe vascular stem-cell tissue known as procambium generates phloem cells on one side and xylem cells on the other. The Arabidopsis PXY gene encodes a leucine-rich repeat receptor-like kinase that is required for polar divisions of procambial cells. The vascular stem-cell tissue known as procambium generates phloem cells on one side and xylem cells on the other. The Arabidopsis PXY gene encodes a leucine-rich repeat receptor-like kinase that is required for polar divisions of procambial cells. As plants elongate and grow, they are faced with two problems: how physically to support their enlarging shoot and how to convey nutrients. Both problems are solved by cells derived from the procambium — a stem-cell population which, in stems, is organized as long ribbons (Figure 1A,B). More specifically, procambium is found in the center of vascular bundles, sandwiched between the xylem and the phloem. Xylem is a tissue that transports water and dissolved minerals, and some xylem cell types produce very thick cell walls that are major contributors to the strength of plant stems. Phloem also functions in long-distance transport, moving sugars, RNA, proteins and other substances. In a typical Arabidopsis flowering stem, a cross section would show about eight vascular bundles, each having a thin band of procambium separating epidermally oriented phloem from centrally oriented xylem (Figure 1B). Vascular bundles connect all parts of the plant, extending from the stem into leaves, and down into the root system. Despite its importance, we know little about how the precise patterning of cell types within a stem's vascular bundle is achieved. This is changing, with a recent paper in Current Biology reporting that the Arabidopsis PXY gene encodes a receptor-like kinase that is required to maintain normal polar cell divisions of the procambium [1Fisher K. Turner S. PXY, a receptor-like kinase essential for maintaining polarity during vascular tissue development in Arabidopsis.Curr. Biol. 2007; 17: 1061-1066Abstract Full Text Full Text PDF PubMed Scopus (250) Google Scholar]. Clues to vascular bundle polarity first came from studies of leaf polarity. Arabidopsis mutants carrying dominant alleles of PHABULOSA (phb-1d) produce radially symmetric needle-like leaves, enveloped by an epidermis corresponding to the top (adaxial surface) of the leaf [2McConnell J.R. Barton M.K. Leaf polarity and meristem formation in Arabidopsis.Development. 1998; 125: 2935-2942PubMed Google Scholar]. Notably, veins of these leaves are also radially symmetric, and the xylem, which is normally toward the top/adaxial leaf surface, completely surrounds the phloem. PHB encodes a member of the class III HD-ZIP gene family, which in Arabidopsis consists of five genes. All the encoded proteins have a start domain which potentially binds a lipid signal, and the mRNAs include an miRNA target site (miR165/166) [3McConnell J.R. Emery J. Eshed Y. Bao N. Bowman J. Barton M.K. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots.Nature. 2001; 411: 709-713Crossref PubMed Scopus (800) Google Scholar, 4Emery J.F. Floyd S.K. Alvarez J. Eshed Y. Hawker N.P. Izhaki A. Baum S.F. Bowman J.L. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes.Curr. Biol. 2003; 13: 1768-1774Abstract Full Text Full Text PDF PubMed Scopus (808) Google Scholar]. PHB is expressed in adaxial tissues of developing organs and in the vascular tissue, and numerous studies using dominant and loss-of-function alleles have revealed roles for three gene family members, PHB, PHV and REV, in specification of adaxial (top) identity [5Kidner C.A. Timmermans M.C.P. Mixing and matching pathways in leaf polarity.Curr. Opin. Plant Biol. 2007; 10: 13-20Crossref PubMed Scopus (65) Google Scholar, 6Prigge M.J. Otsuga D. Alonso J.M. Ecker J.R. Drews G.N. Clark S.E. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development.Plant Cell. 2004; 17: 61-76Crossref PubMed Scopus (518) Google Scholar]. Abaxial (lower surface) identity is specified by KANADI genes, which are expressed in abaxial domains and in phloem [4Emery J.F. Floyd S.K. Alvarez J. Eshed Y. Hawker N.P. Izhaki A. Baum S.F. Bowman J.L. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes.Curr. Biol. 2003; 13: 1768-1774Abstract Full Text Full Text PDF PubMed Scopus (808) Google Scholar, 5Kidner C.A. Timmermans M.C.P. Mixing and matching pathways in leaf polarity.Curr. Opin. Plant Biol. 2007; 10: 13-20Crossref PubMed Scopus (65) Google Scholar, 6Prigge M.J. Otsuga D. Alonso J.M. Ecker J.R. Drews G.N. Clark S.E. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development.Plant Cell. 2004; 17: 61-76Crossref PubMed Scopus (518) Google Scholar, 7Kerstetter R.A. Bollman K. Taylor R.A. Bomblies K. Poethig R.S. KANADI regulates organ polarity in Arabidopsis.Nature. 2001; 411: 706-709Crossref PubMed Scopus (431) Google Scholar]. Adaxial and abaxial-specifying regulators are mutually repressive, as both loss of function mutations and ectopic expression lead to radialized organs. The vascular bundles show reciprocal responses to altered polarity; abaxialized organs produce a radialized phloem-surrounding-xylem phenotype, and adaxialized organs produce a xylem-surrounding-phloem phenotype. An important advance came when the plant's stem was found to use the same polarity signals as the leaf [4Emery J.F. Floyd S.K. Alvarez J. Eshed Y. Hawker N.P. Izhaki A. Baum S.F. Bowman J.L. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes.Curr. Biol. 2003; 13: 1768-1774Abstract Full Text Full Text PDF PubMed Scopus (808) Google Scholar]. The stem's central region corresponds to the adaxial (top) surface, and stems of adaxialized plants also contained radial xylem-surrounding-phloem vascular bundles. Similarly, the periphery of the stem corresponds to the abaxial (bottom) surface, and stems of abaxialized plants also contained radial phloem-surrounding-xylem vascular bundles (Figure 1C). These observations indicate a general role for organ-polarity related cues in patterning vascular bundles. An outstanding question, however, is how directly organ polarity pathways regulate cell types within the vascular bundle. Most radialized organs show distinct and clearly separated zones of xylem and phloem, but strongly abaxialized organs are devoid of vascular bundles [4Emery J.F. Floyd S.K. Alvarez J. Eshed Y. Hawker N.P. Izhaki A. Baum S.F. Bowman J.L. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes.Curr. Biol. 2003; 13: 1768-1774Abstract Full Text Full Text PDF PubMed Scopus (808) Google Scholar, 7Kerstetter R.A. Bollman K. Taylor R.A. Bomblies K. Poethig R.S. KANADI regulates organ polarity in Arabidopsis.Nature. 2001; 411: 706-709Crossref PubMed Scopus (431) Google Scholar]. It might have been predicted, however, that adaxialized vascular bundles would contain only xylem and abaxialized vascular bundles would contain only phloem. One possible explanation is that adaxial identity leads to provascular tissue specification and vascular bundle orientation, while cell types within the bundle itself are patterned using another pathway. Insights into vascular bundle patterning have come from the new study by Fisher and Turner [1Fisher K. Turner S. PXY, a receptor-like kinase essential for maintaining polarity during vascular tissue development in Arabidopsis.Curr. Biol. 2007; 17: 1061-1066Abstract Full Text Full Text PDF PubMed Scopus (250) Google Scholar] on the Arabidopsis pxy mutant. This mutant was notable because its flowering stem contains vascular bundles which are flat, instead of having the triangular shape characteristic of wild-type plants, and because the phloem appears in ectopic positions, intermixed with the xylem (Figure 1C). The mutant vascular bundles contain similar cell numbers as the wild type, and they retain procambium, suggesting a primary defect in cellular organization. However, at least one cell type, metaxylem, is reduced, and pxy veins appear to be poorly aligned along the length of the stem. Detailed analysis showed that procambial cell division patterns are disrupted in the mutant. In the wild type, procambial cells are found in a tight band adjacent to the phloem, and cell divisions along the phloem–xylem axis result in linear cell files separating xylem and phloem. In pxy mutants, the procambial cells are instead found both adjacent to the phloem and deeper within the xylem, and cell division appears randomly oriented. These attributes of the pxy phenotype suggest that the primary role of PXY is to maintain the proper orientation of procambial cell division. PXY encodes a leucine-rich repeat (LRR) receptor-like kinase [1Fisher K. Turner S. PXY, a receptor-like kinase essential for maintaining polarity during vascular tissue development in Arabidopsis.Curr. Biol. 2007; 17: 1061-1066Abstract Full Text Full Text PDF PubMed Scopus (250) Google Scholar]. There is a large family of such kinases in Arabidopsis, with more than 200 members in 15 different subfamilies, yet functions are known for only a small fraction [8Shiu S.H. Blecker A.B. Plant receptor-like kinase gene family: diversity, function, and signaling.Science. 2001; (STKE RE22)Google Scholar]. PXY's closest relatives, the PXY-like genes PXL1 and PXL2, appear to function redundantly with PXY, as double and triple mutants produced enhanced phenotypes. PXY and PXL1,2 are also closely related to CLV1, BAM1, BAM2 and BAM3, which encode LRR receptor-like kinases with functions in another stem cell population — the shoot apical meristem [9Clark S.E. Williams R.W. Meyerowitz E.M. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis.Cell. 1997; 89: 575-585Abstract Full Text Full Text PDF PubMed Scopus (1007) Google Scholar, 10DeYoung B.J. Bickle K.L. Schrage K.J. Muskett P. Patel K. Clark S.E. The CLAVATA1-related BAM1, BAM2, and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis.Plant J. 2006; 45: 1-16Crossref PubMed Scopus (250) Google Scholar]. CLV1 is required to limit the number of shoot apical meristem cell divisions, whereas BAM1, BAM2 and BAM3 appear to promote cell proliferation in the shoot apical meristem. Thus, despite their similar sequences and their requirement for normal meristem (stem cell) function, these proteins carry out distinct signaling roles. More distantly related LRR receptor-like kinases with roles in vascular development have also been identified. VASCULAR HIGHWAY1 (VH1/BRL2), BRL1 and BRL3 encode procambium-expressed LRR receptor-like kinases [11Clay N.K. Nelson T. VH1, a provascular cell-specific receptor kinase that influences leaf cell patterns in Arabidopsis.Plant Cell. 2002; 14: 2707-2722Crossref PubMed Scopus (106) Google Scholar, 12Caño-Delgado A. Yin Y. Yu C. Vafeados D. Mora-Garcia S. Cheng J.-C. Nam K.H. Li J. Chory J. BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis.Development. 2004; 131: 5341-5351Crossref PubMed Scopus (358) Google Scholar]; however, VH1/BRL2 is required for normal phloem function, while BRL1 is required for a normal balance between phloem and xylem cell numbers. The identification of PXY as an LRR receptor-like kinase leads naturally to two questions: what is the ligand, and where is it produced? Attractive candidates are the CLE peptides [13Cock J.M. McCormick S. A large family of genes that share homology with CLAVATA3.Plant Physiol. 2001; 126: 939-942Crossref PubMed Scopus (252) Google Scholar]. The Arabidopsis genome contains 31 CLE genes that encode 26 different CLE peptides, including the putative CLV1 ligand, CLV3 [13Cock J.M. McCormick S. A large family of genes that share homology with CLAVATA3.Plant Physiol. 2001; 126: 939-942Crossref PubMed Scopus (252) Google Scholar, 14Fletcher J.C. Brand U. Running M.P. Simon R. Meyerowitz E.M. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems.Science. 1999; 283: 1911-1914Crossref PubMed Scopus (939) Google Scholar, 15Kondo T. Sawa S. Kinoshita A. Mizuno S. Kakimoto T. Fukuda H. Sakagami Y. A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis.Science. 2006; 313: 845-848Crossref PubMed Scopus (353) Google Scholar, 16Sharma V.K. Ramirez J. Fletcher J.C. The Arabidopsis CLV3-like (CLE) genes are expressed in diverse tissues and encode secreted proteins.Plant Mol. Biol. 2003; 51: 415-425Crossref PubMed Scopus (116) Google Scholar, 17Ito Y. Nakanomyo I. Motose H. Iwamoto K. Sawa S. Dohmae N. Fukuda H. Dodeca-CLE peptide as suppressors of plant stem cell differentiation.Science. 2006; 313: 842-845Crossref PubMed Scopus (441) Google Scholar]. These peptides have diverse expression patterns and activities, including negative regulation of tracheary element differentiation. Other classes of peptide hormones also bind LRR receptor-like kinases, and thus are also candidates for being the PXY ligand [18Matsubayashi Y. Sakagami Y. Peptide hormones in plants.Annu. Rev. Plant Biol. 2006; 57: 649-674Crossref PubMed Scopus (180) Google Scholar]. A non-protein ligand is also possible, an example being brassinolide as the ligand for the LRR receptor-like kinase BRI1 [19Kinoshita T. Caño-Delgado A. Seto H. Hiranuma S. Fujioka S. Yoshida S. an Chory J. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1.Nature. 2005; 433: 167-171Crossref PubMed Scopus (454) Google Scholar]. The identification of PXY as an LRR receptor-like kinase that regulates polar division of procambial cells is a significant step forward in understanding how vascular bundles are patterned. However, the phenotype also raises interesting questions. For example, in pxy mutants, phloem cells can be found embedded within the xylem, with no adjacent phloem neighbors [1Fisher K. Turner S. PXY, a receptor-like kinase essential for maintaining polarity during vascular tissue development in Arabidopsis.Curr. Biol. 2007; 17: 1061-1066Abstract Full Text Full Text PDF PubMed Scopus (250) Google Scholar]. One possible explanation for this is that PXY is also required to inhibit phloem identity, but this seems unlikely as phloem cell numbers are not elevated in pxy mutants. Alternatively, this observation might mean that phloem is specified by a lineage-dependent mechanism, rather than by positional signaling [20Scheres B. Plant cell identity. The role of position and lineage.Plant Physiol. 2001; 125: 112-114Crossref PubMed Scopus (61) Google Scholar]. Determining the association of ectopic phloem and procambial cells, and whether ectopic phloem cells are parts of phloem cell files along the vein's long axis may coax this PXY to reveal even more secrets.
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