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GLABROUS INFLORESCENCE STEMS regulates trichome branching by genetically interacting with SIM in Arabidopsis

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Abstract

Arabidopsis trichomes are large branched single cells that protrude from the epidermis. The first morphological indication of trichome development is an increase in nuclear content resulting from an initial cycle of endoreduplication. Our previous study has shown that the C2H2 zinc finger protein GLABROUS INFLORESCENCE STEMS (GIS) is required for trichome initiation in the inflorescence organ and for trichome branching in response to gibberellic acid signaling, although GIS gene does not play a direct role in regulating trichome cell division. Here, we describe a novel role of GIS, controlling trichome cell division indirectly by interacting genetically with a key endoreduplication regulator SIAMESE (SIM). Our molecular and genetic studies have shown that GIS might indireclty control cell division and trichome branching by acting downstream of SIM. A loss of function mutation of SIM signficantly reduced the expression of GIS. Futhermore, the overexpression of GIS rescued the trichome cluster cell phenotypes of sim mutant. The gain or loss of function of GIS had no significant effect on the expression of SIM. These results suggest that GIS may play an indirect role in regulating trichome cell division by genetically interacting with SIM.

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References

  • An, L., Zhou, Z., Su, S., Yan, A., Gan, Y., 2012. GLABROUS INFLORESCENCE STEMS (GIS) is required for trichome branching through gibberellic acid signaling in Arabidopsis. Plant Cell Physiol., 53(2):457–469. [doi:10.1093/pcp/pcr192]

    Article  PubMed  CAS  Google Scholar 

  • Bao, S.J., An, L.J., Su, S., Zhou, Z.J., Gan, Y.B., 2011. Expression patterns of nitrate, phosphate, and sulfate transporters in Arabidopsis roots exposed to different nutritional regimes. Botany-Botanique, 89(9):647–653. [doi:10.1139/B11-053]

    Article  CAS  Google Scholar 

  • Bertram, J.G., Bloom, L.B., Turner, J., O’donnell, M., Beechem, J.M., Goodman, M.F., 1998. Pre-steady state analysis of the assembly of wild type and mutant circular clamps of Escherichia coli DNA polymerase III onto DNA. J. Biol. Chem., 273(38):24564–24574. [doi:10.1074/jbc.273.38.24564]

    Article  PubMed  CAS  Google Scholar 

  • Bramsiepe, J., Wester, K., Weinl, C., Roodbarkelari, F., Kasili, R., Larkin, J.C., Hulskamp, M., Schnittger, A., 2010. Endoreplication controls cell fate maintenance. PLoS Genet., 6(6):e1000996. [doi:10.1371/journal.pgen.1000 996]

    Article  PubMed  Google Scholar 

  • Cebolla, A., Vinardell, J.M., Kiss, E., Olah, B., Roudier, F., Kondorosi, A., Kondorosi, E., 1999. The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J., 18(16): 4476–4484. [doi:10.1093/emboj/18.16.4476]

    Article  PubMed  CAS  Google Scholar 

  • Churchman, M.L., Brown, M.L., Kato, N., Kirik, V., Hulskamp, M., Inze, D., de Veylder, L., Walker, J.D., Zheng, Z., Oppenheimer, D.G., et al., 2006. SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. Plant Cell, 18(11): 3145–3157. [doi:10.1105/tpc.106.044834]

    Article  PubMed  CAS  Google Scholar 

  • Clough, S.J., Bent, A.F., 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J., 16(6):735–743. [doi:10.1046/j.1365-313x.1998.00343.x]

    Article  PubMed  CAS  Google Scholar 

  • Folkers, U., Berger, J., Hulskamp, M., 1997. Cell morphogenesis of trichomes in Arabidopsis: differential control of primary and secondary branching by branch initiation regulators and cell growth. Development, 124(19): 3779–3786.

    PubMed  CAS  Google Scholar 

  • Gan, Y.B., Filleur, S., Rahman, A., Gotensparre, S., Forde, B.G., 2005. Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana. Planta, 222(4):730–742. [doi:10.1007/s00425-005-0020-3]

    Article  PubMed  CAS  Google Scholar 

  • Gan, Y.B., Kumimoto, R., Liu, C., Ratcliffe, O., Yu, H., Broun, P., 2006. GLABROUS INFLORESCENCE STEMS modulates the regulation by gibberellins of epidermal differentiation and shoot maturation in Arabidopsis. Plant Cell, 18(6):1383–1395. [doi:10.1105/tpc.106.041533]

    Article  PubMed  CAS  Google Scholar 

  • Gan, Y.B., Liu, C., Yu, H., Broun, P., 2007. Integration of cytokinin and gibberellin signalling by Arabidopsis transcription factors GIS, ZFP8 and GIS2 in the regulation of epidermal cell fate. Development, 134(11):2073–2081. [doi:10.1242/dev.005017]

    Article  PubMed  CAS  Google Scholar 

  • Gan, Y.B., Zhou, Z.J., An, L.J., Bao, S.J., Liu, Q., Srinivasan, M., Goddard, P., 2010. The effects of fluctuations in the nutrient supply on the expression of ANR1 and 11 other MADS box genes in shoots and roots of Arabidopsis thaliana. Botany-Botanique, 88(12):1023–1031. [doi:10.1139/B10-075]

    Article  CAS  Google Scholar 

  • Gan, Y.B., Zhou, Z.J., An, L.J., Bao, S.J., Forde, B.G., 2011. A comparison between northern blotting and quantitative real-time PCR as a means of detecting the nutritional regulation of genes expressed in roots of Arabidopsis thaliana. Agric. Sci. China, 10(3):335–342. [doi:10.1016/S1671-2927(11)60012-6]

    Article  CAS  Google Scholar 

  • Hülskamp, M., Misra, S., Jurgens, G., 1994. Genetic dissection of trichome cell development in Arabidopsis. Cell, 76(3):555–566. [doi:10.1016/0092-8674(94)90118-X]

    Article  PubMed  Google Scholar 

  • Hülskamp, M., Schnittger, A., Folkers, U., 1999. Pattern formation and cell differentiation: trichomes in Arabidopsis as a genetic model system. Int. Rev. Cytol., 186:147–178. [doi:10.1016/S0074-7696(08)61053-0]

    Article  PubMed  Google Scholar 

  • Ilgenfritz, H., Bouyer, D., Schnittger, A., Mathur, J., Kirik, V., Schwab, B., Chua, N.H., Jurgens, G., Hulskamp, M., 2003. The Arabidopsis STICHEL gene is a regulator of trichome branch number and encodes a novel protein. Plant Physiol., 131(2):643–655. [doi:10.1104/pp.014209]

    Article  PubMed  CAS  Google Scholar 

  • Ishida, T., Kurata, T., Okada, K., Wada, T., 2008. A genetic regulatory network in the development of trichomes and root hairs. Annu. Rev. Plant. Biol., 59:365–386. [doi:10.1146/annurev.arplant.59.032607.092949]

    Article  PubMed  CAS  Google Scholar 

  • Johnson, H.B., 1975. Plant pubescence: an ecological perspective. Bot. Rev., 41(3):233–258. [doi:10.1007/BF02860838]

    Article  Google Scholar 

  • Kasili, R., Walker, J.D., Simmons, L.A., Zhou, J., de Veylder, L., Larkin, J.C., 2010. SIAMESE cooperates with the CDH1-like protein CCS52A1 to establish endoreplication in Arabidopsis thaliana trichomes. Genetics, 185(1): 257–268. [doi:10.1534/genetics.109.113274]

    Article  PubMed  CAS  Google Scholar 

  • Larkin, J.C., Brown, M.L., Schiefelbein, J., 2003. How do cells know what they want to be when they grow up? Lessons from epidermal patterning in Arabidopsis. Annu. Rev. Plant Biol., 54:403–430. [doi:10.1146/annurev.arplant.54.031902.134823]

    Article  PubMed  CAS  Google Scholar 

  • Lilly, M.A., Duronio, R.J., 2005. New insights into cell cycle control from the Drosophila endocycle. Oncogene, 24(17):2765–2775. [doi:10.1038/sj.onc.1208610]

    Article  PubMed  CAS  Google Scholar 

  • Luo, D., Oppenheimer, D.G., 1999. Genetic control of trichome branch number in Arabidopsis: the roles of the FURCA loci. Development, 126(24):5547–5557.

    PubMed  CAS  Google Scholar 

  • Marks, M.D., 1997. Molecular genetic analysis of trichome development in Arabidopsis. Annu. Rev. Plant Physiol. Plant Mol. Biol., 48:137–163. [doi:10.1146/annurev.arplant.48.1.137]

    Article  PubMed  CAS  Google Scholar 

  • Payne, C.T., Zhang, F., Lloyd, A.M., 2000. GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics, 156(3):1349–1362.

    PubMed  CAS  Google Scholar 

  • Plett, J.M., Mathur, J., Regan, S., 2009. Ethylene receptor ETR2 controls trichome branching by regulating microtubule assembly in Arabidopsis thaliana. J. Exp. Bot., 60(13):3923–3933. [doi:10.1093/jxb/erp228]

    Article  PubMed  CAS  Google Scholar 

  • Rao, K.N., Venkatachalam, S.R., 1999. Dihydrofolate reductase and cell growth activity inhibition by the β-carboline-benzoquinolizidine plant alkaloid deoxytubulosine from Alangium lamarckii: its potential as an antimicrobial and anticancer agent. Bioorg. Med. Chem., 7(6):1105–1110. [doi:10.1016/S0968-0896(98)00262-4]

    Article  PubMed  CAS  Google Scholar 

  • Rodney, M., Mark, R.D., 1997. Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution, 51:1435–1444.

    Article  Google Scholar 

  • Schellmann, S., Schnittger, A., Kirik, V., Wada, T., Okada, K., Beermann, A., Thumfahrt, J., Jurgens, G., Hülskamp, M., 2002. TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J., 21(19):5036–5046. [doi:10.1093/emboj/cdf524]

    Article  PubMed  CAS  Google Scholar 

  • Schnittger, A., Schobinger, U., Bouyer, D., Weinl, C., Stierhof, Y.D., Hülskamp, M., 2002a. Ectopic D-type cyclin expression induces not only DNA replication but also cell division in Arabidopsis trichomes. PNAS, 99(9): 6410–6415. [doi:10.1073/pnas.092657299]

    Article  PubMed  CAS  Google Scholar 

  • Schnittger, A., Schobinger, U., Stierhof, Y.D., Hülskamp, M., 2002b. Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Curr. Biol., 12(5):415–420. [doi:10.1016/S0960-9822(02)00693-0]

    Article  PubMed  CAS  Google Scholar 

  • Szymanski, D.B., Marks, M.D., 1998. GLABROUS1 overexpression and TRIPTYCHON alter the cell cycle and trichome cell fate in Arabidopsis. Plant Cell, 10(12): 2047–2062. [doi:10.1105/tpc.10.12.2047]

    PubMed  CAS  Google Scholar 

  • Tominaga-Wada, R., Ishida, T., Wada, T., 2011. New Insights into the Mechanism of Development of Arabidopsis Root Hairs and Trichomes. In: Jeon, K.W. (Ed.), International Review of Cell and Molecular Biology, 286:67–106.

    Article  PubMed  CAS  Google Scholar 

  • Walker, J.D., Oppenheimer, D.G., Concienne, J., Larkin, J.C., 2000. SIAMESE, a gene controlling the endoreduplication cell cycle in Arabidopsis thaliana trichomes. Development, 127(18):3931–3940.

    PubMed  CAS  Google Scholar 

  • Weinl, C., Marquardt, S., Kuijt, S.J., Nowack, M.K., Jakoby, M.J., Hulskamp, M., Schnittger, A., 2005. Novel functions of plant cyclin-dependent kinase inhibitors, ICK1/KRP1, can act non-cell-autonomously and inhibit entry into mitosis. Plant Cell, 17(6):1704–1722. [doi:10.1105/tpc.104.030486]

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Yin-bo Gan.

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Project supported by the National Natural Science Foundation of China (Nos. 30970167 and 31228002), the Zhejiang Qianjiang Talent Program (No. 2010R10084), the Zhejiang Provincial Natural Science Foundation of China (No. Z31100041), and the Zhejiang Province Foundation for Returned Scholars (No. 20100129), China

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Sun, Ll., Zhou, Zj., An, Lj. et al. GLABROUS INFLORESCENCE STEMS regulates trichome branching by genetically interacting with SIM in Arabidopsis . J. Zhejiang Univ. Sci. B 14, 563–569 (2013). https://doi.org/10.1631/jzus.B1200349

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  • DOI: https://doi.org/10.1631/jzus.B1200349

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