Advertisement

Plant Molecular Biology Reporter

, Volume 33, Issue 5, pp 1441–1450 | Cite as

Isolation and Functional Analysis of SpWOX13 from Stipa purpurea

  • Xudong Sun
  • Nan Xiang
  • Chongde Wang
  • Shihai Yang
  • Xiong Li
  • Yunqiang Yang
  • Yongping Yang
Original Paper

Abstract

Members of the WUSCHEL-related homeobox (WOX) gene family encode plant-specific transcription factors that play key roles in controlling gene expression at all stages of plant development. In the present study, we isolated and characterized SpWOX13 (GenBank accession no. KJ713172), a member of the WOX gene family, from Stipa purpurea. Sequence and phylogenetic analyses showed that SpWOX13 belongs to an ancient clade of WOX genes. A subcellular localization analysis indicated that SpWOX13 localizes in the nucleus. The transcript levels of SpWOX13 were higher in young leaves and the vegetative apex than in other tissues of S. purpurea. Ectopic expression of SpWOX13 in Arabidopsis resulted in late flowering plants as these showed more rosette leaves. Histological analyses of the transgenic plants showed aberrant arrangements in the tunica cell layers of the shoot apical meristem. Scanning electron microscopy analyses revealed that the leaf pavement cells were larger in SpWOX13-overexpressing transgenic plants than in wild type. Our results suggest that SpWOX13 is involved in delaying and/or inhibiting cell differentiation.

Keywords

SpWOX13 Transcription factor Cell differentiation Stipa purpurea Arabidopsis 

Notes

Acknowledgments

This work was financially supported by the Major state Basic Research Development Program of China (2010CB951704) and grants from the National Natural Science Foundation of China (NSFC) (41271058) to Y. P. Yang and from the NSFC (31400244) to X.D. Sun.

References

  1. Bai X, Long J, He X, Li S, Xu H (2014) Molecular cloning and characterization of pathogenesis-related protein family 10 gene from spinach (SoPR10). Biosci, Biotechnol, Biochem. doi: 10.1080/09168451.09162014.09910094 Google Scholar
  2. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  3. Deveaux Y, Toffano-Nioche C, Claisse G, Thareau V, Morin H, Laufs P, Moreau H, Kreis M, Lecharny A (2008) Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evol Biol 8:291PubMedCentralCrossRefPubMedGoogle Scholar
  4. Etchells JP, Provost CM, Mishra L, Turner SR (2013) WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation. Development 140:2224–2234PubMedCentralCrossRefPubMedGoogle Scholar
  5. Fleming AJ (2005) The control of leaf development. New Phytol 166:9–20CrossRefPubMedGoogle Scholar
  6. Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z (2005) Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120:687–700CrossRefPubMedGoogle Scholar
  7. Haecker A, Laux T (2001) Cell-cell signaling in the shoot meristem. Curr Opin Plant Biol 4:441–446CrossRefPubMedGoogle Scholar
  8. Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–668CrossRefPubMedGoogle Scholar
  9. Horiguchi G, Ferjani A, Fujikura U, Tsukaya H (2006) Coordination of cell proliferation and cell expansion in the control of leaf size in Arabidopsis thaliana. J Plant Res 119:37–42CrossRefPubMedGoogle Scholar
  10. Kamiya N, Nagasaki H, Morikami A, Sato Y, Matsuoka M (2003) Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. Plant J 35:429–441CrossRefPubMedGoogle Scholar
  11. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965CrossRefPubMedGoogle Scholar
  12. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962CrossRefPubMedGoogle Scholar
  13. Lian G, Ding Z, Wang Q, Zhang D, Xu J (2014) Origins and evolution of WUSCHEL-related homeobox protein family in plant kingdom. Sci World J 2014:534140CrossRefGoogle Scholar
  14. Liu J, Sheng L, Xu Y, Li J, Yang Z, Huang H, Xu L (2014) WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell 26:1081–1093PubMedCentralCrossRefPubMedGoogle Scholar
  15. Matsumoto N, Okada K (2001) A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev 15:3355–3364PubMedCentralCrossRefPubMedGoogle Scholar
  16. Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815CrossRefPubMedGoogle Scholar
  17. Nardmann J, Werr W (2012) The invention of WUS-like stem cell-promoting functions in plants predates leptosporangiate ferns. Plant Mol Biol 78:123–134CrossRefPubMedGoogle Scholar
  18. Nardmann J, Ji J, Werr W, Scanlon MJ (2004) The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 131:2827–2839CrossRefPubMedGoogle Scholar
  19. Nardmann J, Reisewitz P, Werr W (2009) Discrete shoot and root stem cell-promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Mol Biol Evol 26:1745–1755CrossRefPubMedGoogle Scholar
  20. Romera-Branchat M, Ripoll JJ, Yanofsky MF, Pelaz S (2012) The WOX13 homeobox gene promotes replum formation in the Arabidopsis thaliana fruit. Plant J 73:37–49CrossRefPubMedGoogle Scholar
  21. Sakakibara K, Reisewitz P, Aoyama T, Friedrich T, Ando S, Sato Y, Tamada Y, Nishiyama T, Hiwatashi Y, Kurata T, Ishikawa M, Deguchi H, Rensing SA, Werr W, Murata T, Hasebe M, Laux T (2014) WOX13-like genes are required for reprogramming of leaf and protoplast cells into stem cells in the moss Physcomitrella patens. Development 141:1660–1670CrossRefPubMedGoogle Scholar
  22. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814CrossRefPubMedGoogle Scholar
  23. Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644CrossRefPubMedGoogle Scholar
  24. Shimizu R, Ji J, Kelsey E, Ohtsu K, Schnable PS, Scanlon MJ (2009) Tissue specificity and evolution of meristematic WOX3 function. Plant Physiol 149:841–850PubMedCentralCrossRefPubMedGoogle Scholar
  25. Su YH, Zhao XY, Liu YB, Zhang CL, O'Neill SD, Zhang XS (2009) Auxin-induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. Plant J 59:448–460PubMedCentralCrossRefPubMedGoogle Scholar
  26. Sun XD, Feng ZH, Meng LS (2012) Ectopic expression of the Arabidopsis ASYMMETRIC LEAVES2-LIKE5 (ASL5) gene in cockscomb (Celosia cristata) generates vascular-pattern modifications in lateral organs. Plant Cell Tiss Organ Cult 110:163–169CrossRefGoogle Scholar
  27. Sun XD, Feng ZH, Meng LS, Zhu J, Geitmann A (2013) Arabidopsis ASL11/LBD15 is involved in shoot apical meristem development and regulates WUS expression. Planta 237:1367–1378CrossRefPubMedGoogle Scholar
  28. Sun X, Guan Y, Hu X (2014) Isolation and characterization of IaYABBY2 gene from Incarvillea arguta. Plant Mol Biol Report. doi: 10.1007/s11105-11014-10725-11101 PubMedCentralGoogle Scholar
  29. Tsukaya H (2008) Controlling size in multicellular organs: focus on the leaf. PLoS Biol 6:e174PubMedCentralCrossRefPubMedGoogle Scholar
  30. Ueda M, Zhang Z, Laux T (2011) Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev Cell 20:264–270CrossRefPubMedGoogle Scholar
  31. van der Graaff E, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10:248PubMedCentralCrossRefPubMedGoogle Scholar
  32. Wang J, Kucukoglu M, Zhang L, Chen P, Decker D, Nilsson O, Jones B, Sandberg G, Zheng B (2013) The Arabidopsis LRR-RLK, PXC1, is a regulator of secondary wall formation correlated with the TDIF-PXY/TDR-WOX4 signaling pathway. BMC Plant Biol 13:94PubMedCentralCrossRefPubMedGoogle Scholar
  33. Wu X, Dabi T, Weigel D (2005) Requirement of homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance. Curr Biol 15:436–440CrossRefPubMedGoogle Scholar
  34. Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Xudong Sun
    • 1
    • 2
    • 3
  • Nan Xiang
    • 1
    • 2
    • 3
  • Chongde Wang
    • 6
  • Shihai Yang
    • 4
    • 5
  • Xiong Li
    • 1
    • 2
    • 3
    • 4
  • Yunqiang Yang
    • 1
    • 2
    • 3
    • 4
  • Yongping Yang
    • 1
    • 2
    • 3
  1. 1.Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of BotanyChinese Academy of SciencesKunmingChina
  2. 2.Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species, Kunming Institute of BotanyChinese Academy of SciencesKunmingChina
  3. 3.Institute of Tibetan Plateau Research at Kunming, Kunming Institute of BotanyChinese Academy of SciencesKunmingChina
  4. 4.University of the Chinese Academy of SciencesBeijingChina
  5. 5.Institute of Tibetan Plateau ResearchChinese Academy of SciencesBeijingChina
  6. 6.College of Plant ProtectionYunnan Agriculture UniversityKunmingChina

Personalised recommendations