Abstract
Secondary growth is supported by a dividing population of meristematic cells within the vascular cambium whose daughter cells are recruited to differentiate within secondary phloem and xylem tissues. We cloned a Populus Class 1 KNOX homeobox gene, ARBORKNOX1 (ARK1), which is orthologous to Arabidopsis SHOOT MERISTEMLESS (STM). ARK1 is expressed in the shoot apical meristem (SAM) and the vascular cambium, and is down-regulated in the terminally differentiated cells of leaves and secondary vascular tissues that are derived from these meristems. Transformation of Populus with either ARK1 or STM over-expression constructs results in similar morphological phenotypes characterized by inhibition of the differentiation of leaves, internode elongation, and secondary vascular cell types in stems. Microarray analysis showed that 41% of genes up-regulated in the stems of ARK1 over-expressing plants encode proteins involved in extracellular matrix synthesis or modification, including proteins involved in cell identity and signaling, cell adhesion, or cell differentiation. These gene expression differences are reflected in alterations of cell wall biochemistry and lignin composition in ARK1 over-expressing plants. Our results suggest that ARK1 has a complex mode of action that may include regulating cell fates through modification of the extracellular matrix. Our findings support the hypothesis that the SAM and vascular cambium are regulated by overlapping genetic programs.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Acosta-Garcia G, Vielle-Calzada JP (2004) A classical Arabinogalactan protein is essential for the initiation of female gametogenesis in Arabidopsis. Plant Cell 16:2614–2628
Baluska F, Samaj J, Wojtazek P, Volmann D, Menzel D (2003) Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. Plant Phys 133:482–491
Busov V, Meilan R, Pearce D, Ma C, Rood S, Strauss S (2003) Activation tagging of a dominant gibberellin catabolism gene (GA 2-oxidase) from poplar that regulates tree stature. Plant Phys 123:1283–1291
Byrne M, Groover A, Fontana J, Martienssen R (2003) Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER. Development 130:3941–3950
Chen H, Banerjee A, Hannapel D (2004) The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1. Plant J 38:276–284
Chuck G, Lincoln C, Hake S (1996) KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8:1277–1289
Ehlting J, Mattheus N, Aeschliman DS, Li E, Hamberger B, Cullis( IF, Zhuang J, Kaneda M, Mansfield SD, Samuels AL, Ritland K, Ellis BE, Bohlmann J Douglas CJ (2005) Global transcript profiling of primary stems from Arabidopsis thaliana identifies candidate genes for missing links in lignin biosynthesis and transcriptional regulators of fiber differentiation. Plant J 42:618–640
Emery J, Floyd S, Alvarez J, Eshed Y, Hawker N, Izhaki A, Baum S, Bowman J (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 14:1768–1774
Franke R, McMichael CM, Meyer K, Shirley AM, Cusumano JC, Chapple C (2000) Modified lignin in tobacco and poplar plants over-expressing the Arabidopsis gene encoding ferulate 5-hydroxylase. Plant J 22:223–234
Gallois J, Woodward C, Reddy G, Sablowski R (2002) Combined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic organogenesis in Arabidopsis. Development 129:3207–3217
Ganfornina M, Sanchez D (1999) Generation of evolutionary novelty by functional shift. BioEssays 21:432–439
Gleave AP (1992) A versatile binary vector system with a T-DNA organizational structure conducive to efficient integration of cloned DNA into the Plant Genome. Plant Mol Biol 6:1203–1207
Groover A (2005) What genes make a tree a tree? Trends Plant Sci 10:210–214
Groover A, Fontana J, Dupper G, Ma C, Martienssen R, Strauss S, Meilan R (2004) Gene and enhancer trap tagging of vascular-expressed genes in poplar trees. Plant Phys 134:1742–1751
Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucl. Acids Symp Ser 41:95–98
Han K, Meilan R, Ma C, Strauss S (2000) An Agrobacterium transformation protocol effective in a variety of cottonwood hybrids (genus Populus). Plant Cell Rep 19:315–320
Hay A, Kaur H, Phillips A, Hedden P, Hake S, Tsiantis M (2002) The gibberellin pathway mediates KNOTTED1-Type homeobox functions in plants with diverse body plans. Curr Biol 12:1557–1565
Huntley SK, Ellis D, Gilbert M, Chapple C, Mansfield SD (2003) Improved pulping efficiency in C4H-F5H transformed poplar. J Agr Food Chem 51:6178–6183
Johnson K, Jones B, Bacic A, Schultz C (2003) The fasciclin-like arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules. Plant Phys 133:1911–1925
Ko J, Han K (2004) Arabidopsis whole-transcriptome profiling defines the features of coordinated regulations that occur during secondary growth. Plant Mol Biol 55:433–453
Lafarguette F, Leple J, Dejardin A, Laurans F, Consta G, Lesage-Descauses M, Pilate G (2004) Poplar genes encoding fasciclin-like arabinogalactan proteins are highly expressed in tension wood. New Phyt 164:107–121
Lapierre C, Pollet B, Petit-Conil M, Toval G, Romero J, Pilate G, Leple JC, Boerjan W, Ferret VV, De Nadai V, Jouanin L (1999) Structural alterations of lignins in transgenic poplars with depressed cinnamyl alcohol dehydrogenase or caffeic acid O-methyltransferase activity have an opposite impact on the efficiency of industrial kraft pulping. Plant Phys 119:153–164
Larson P (1994) The vascular cambium. Springer-Verlag, NY
Laux T, Mayer K, Berger J, Jurgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96
Lenhard M, Jurgens G, Laux T (2002) The WUSHEL and SHOOT MERISTEMLESS genes fufil complementary roles in Arabidopsis shoot meristem regulation. Development 129:3195–3206
Long JA, Moan E, Medford J, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69
Long JA, Barton MK (1998) The development of apical embryonic pattern in Arabidopsis. Development 125:3027–3035
Mayer K, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Role of WUSHCEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815
Mele G, Ori N, Sato Y, Hake S (2003) The Knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulation metabolic pathways. Genes Dev 17:2088–2093
Rogers L, Campbell M (2004) The genetic control of lignin deposition during plant growth and development. New Phyt 164:17–30
Pien S, Wyrzykowska J, McQueen-Mason S, Smart C, Fleming A (2001) Local expression of expansin induces the entire process of leaf development and modified leaf shape. Proc Natl Acad Sci USA 98:11812–11817
Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press, NY
Sakamoto T, Kamiya N, Ueguchi-Tanaka M, Iwahori S, Matsuoka M (2001) KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev 15:581–590
Schrader J, Nilsson J, Mellerowicz E, Berglund A, Nilsson P, Hertzberg M, Sandberg G (2004) A high-resolution transcript profile across the wood-forming meristem of poplar identifies potential regulators of cambial stem cell identity. Plant Cell 16:2278–2292
Sinha N, Williams R, Hake S (1993) Overexpression of the maize homeobox gene, Kn1, causes a switch from determinant to indeterminate cell fates. Genes Dev 7:787–795
Smith H, Hake S (2003) The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis inflorescence. Plant Cell 15:1717–1727
Sterky F, Bhalerao RR, Unneberg P, Segerman B, Nilsson P, Brunner AM, Charbonnel-Campaa L, Lindvall JJ, Tandre K, Strauss SH, Sundberg B, Gustafsson P, Uhlen M, Bhalerao RP, Nilsson O, Sandberg G, Karlsson J, Lundeberg J, Jansson S (2004) A Populus EST resource for plant functional genomics. Proc Natl Acad Sci USA 101:13951–13956
Vollbrecht E, Veit B, Sinha N, Hake S (1991) The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350:241–243
Williams R (1998) Plant homeobox genes: many functions stem from a common motif. BioEssays 20:280–282
Wiweger M, Farbos I, Ingouff M, Lagercrantz U, von Arnold S (2003) Expression of Chia4-Pa chitinase genes during somatic and zygotic embryo development in Norway spruce (Picea abies): similarities and differences between gymnosperm and angiosperm class IV chitinases. J Exp Bot 54: 2691–2699
Zhong R, Kays S, Schroeder B, Ye Z (2002) Mutation of a chitinase-like gene causes extopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 14:165–179
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was supported by the USDA Forest Service and USDA NRI Grant 2003-00664 to AG, and a grants from the U.S. Department of Energy, Office of Science, Biological and Environmental Research Carbon Sequestration Program to AG and SD.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Groover, A.T., Mansfield, S.D., DiFazio, S.P. et al. The Populus homeobox gene ARBORKNOX1 reveals overlapping mechanisms regulating the shoot apical meristem and the vascular cambium. Plant Mol Biol 61, 917–932 (2006). https://doi.org/10.1007/s11103-006-0059-y
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11103-006-0059-y