Functional Complementation Studies and Analysis of Downstream Regulatory Gene Expression Networks of Trichome Trimeric Complex

  • Anh Phu Nam Bui Division of Biotechnology, Institute of Agricultural Sciences for Southern Vietnam, 121 Nguyen-Binh-Khiem Street, District 01, Ho Chi Minh city 71007, Vietnam, Department of Cell Biology, Texas Tech University Health Sciences Center, 3601 4th street, Lubbock, Texas 79430, USA
  • Vimal Kumar Balasubramanian Pacific Northwest National Laboratory, 902 Battelle Blvd, Richland, WA 99354, USA
  • Thuan-Anh Nguyen-Huu Faculty of Biotechnology, Nguyen Tat Thanh University, 298A-300A Nguyen Tat Thanh Street, Ward 13, District 4, Ho Chi Minh city 72820, Vietnam
  • Tuan-Loc Le Faculty of Biotechnology, Nguyen Tat Thanh University, 298A-300A Nguyen Tat Thanh Street, Ward 13, District 4, Ho Chi Minh city 72820, Vietnam
  • Hoang Dung Tran Faculty of Biotechnology, Nguyen Tat Thanh University, 298A-300A Nguyen Tat Thanh Street, Ward 13, District 4, Ho Chi Minh city 72820, Vietnam
Keywords: Arabidopsis, trichome, MYB2, TTG3, DEL65, DEL61, A genome, D genomes

Abstract

In Arabidopsis, previous genetic analysis has revealed that trichome initiation is positively mediated by a trimeric activation complex comprised of an R2R3-MYB protein GLABRA1 (GL1), a basic helix-loop-helix (bHLH) GLABRA3 (GL3) which acts redundantly with its close homolog ENHANCER OF GLABRA3 (EGL3), and a WD40 protein TRANSPARENT TESTA GLABRA1 (TTG1). We studied the functionality of four individual cotton genes MYB2, TTG3, DEL65 and DEL61 from diploid cotton A and D genomes, which show high similarity in sequence with GL1, TTG1, GL3 and EGL3, respectively, in their respective Arabidopsis glabrous mutants. Our complementation assays proved that transgenic lines with MYB2, TTG3 from diploid genomes A and D could rescue the trichomeless phenotype of gl1-1 and ttg1-1, respectively. However, DEL61 from both the species could not rescue this phenotype of gl3-1 egl3-77439 double mutant. Interestingly, the DEL65 from A species rescued gl3-1 egl3-77439 double mutant but not from D diploid species. Comparative quantitative PCR analysis of the downstream regulatory network genes showed a similar pattern for MYB, TTG3 complemented lines from A- and D- diploid species. Comparative analysis of the DEL65 from A- (rescued the trichomeless phenotype) and D- (did not rescued the trichomeless phenotype) showed differential expression of regulatory network genes between these two lines. These results suggested that MYB2, TTG3 and DEL65, when expressed in Arabidopsis, regulated the regulatory network genes during the trichome initiation process.

References

. M. Hülskamp, S. Miséra and G. Jürgens. “Genetic dissection of trichome cell development in Arabidopsis.”: Cell, vol. 76, pp. 555-566, Feb. 1994.

. D.B. Szymanski, R.A. Jilk, S.M. Pollock and M.D. Marks, “Control of GL2 expression in Arabidopsis leaves and trichomes.” Development, 125, pp. 1161-1171, 1998.

. J.C. Larkin, M.L. Brown and J. Schiefelbein. “How do cells know what they want to be when they grow up? Lessons from Epidermal Patterning in Arabidopsis.” Annu Rev Plant Biol, vol. 54, pp. 403-430, Jun. 2003.

. L. Serna and C. Martin. “Trichomes: different regulatory networks lead to convergent structures.” Trends Plant Sci, vol. 11, pp. 274-280, Jun. 2006.

. A.R. Walker, P.A. Davison, A.C. Bolognesi-Winfield, C.M. James, N. Srinivasan, T.L. Blundell, J.J. Esch, M.D. Marks and J.C. Gray. “The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein.” Plant Cell, vol. 11, pp. 1337-1350, Jul. 1999.

. B.J. Glover. “Differentiation in plant epidermal cells.” J Exp Bot, vol. 51, pp. 497-505, Mar. 2000.

. J. Schiefelbein. “Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot.” Curr Opin Plant Biol, vol. 6, pp. 74-78, Feb. 2003.

. N.A. Ramsay and B.J. Glover. “MYB–bHLH–WD40 protein complex and the evolution of cellular diversity.” Trends Plant Sci, vol. 10, pp. 63-70, Feb. 2005.

. D.G. Oppenheimer and P.L. Herman, S. Sivakumaran, J.Esch and M.D. Marks. “A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules.” Cell, vol. 67, pp. 483-493, Nov. 1991.

. C.T. Payne, F. Zhang and A.M. Lloyd. “GL3 Encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1.” Genetics, vol. 156, pp. 1349-1362, Nov. 2000.

. F. Zhang, A. Gonzalez, M. Zhao, C.T. Payne and A. Lloyd. “A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis.” Development, vol. 130, pp. 4859-4869, 2003.

. M. Hulskamp. “Plant trichomes: a model for cell differentiation.” Nat Rev Mol Cell Biol, vol. 5, pp. 471-480, Jun. 2004.

. A.L. Serna. “Network of interacting factors triggering different cell fates.” Plant Cell, vol. 16, pp. 2258-2263, Sep. 2004.

. S. Schellmann, A. Schnittger, V. Kirik, T. Wada, K. Okada, A. Beermann, J. Thumfahrt, G. Jürgens and M. Hülskamp. “TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis.” EMBO J, vol. 21, pp. 5036-5046, Oct. 2002.

. V. Kirik, M. Simon, M. Huelskamp and J. Schiefelbein. “The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis.” Dev Biol, vol. 268, pp. 506-513, Apr. 2004.

. V. Kirik, M. Simon, K. Wester, J. Schiefelbein and M. Hulskamp. “ENHANCER of TRY and CPC 2 (ETC2) reveals redundancy in the region-specific control of trichome development of Arabidopsis.” Plant Mol Biol, vol. 55, pp. 389-398, May. 2004.

. R. Tominaga, M. Iwata, R. Sano, K. Inoue, K. Okada and T. Wada. “Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation.” Development, vol. 135, pp. 1335-1345, 2008.

. S. Wang, S.H. Kwak, Q. Zeng, B.E. Ellis, X.Y. Chen, J. Schiefelbein and J.G. Chen. “TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis.” Development, vol. 134, pp. 3873-3882, 2007.

. S. Wang, L. Hubbard, Y. Chang, J. Guo, J. Schiefelbein and J.–G. Chen. “Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis.” BMC Plant Biology, vol. 8, Jul. 2008.

. K. Wester, S. Digiuni, F. Geier, J. Timmer, C. Fleck and M. Hülskamp. “Functional diversity of R3 single-repeat genes in trichome development.” Development, vol. 136, pp. 1487-1496, 2009.

. P.A. Fryxell, L.A. Craven and J.M. Stewart. “A Revision of Gossypium Sect. Grandicalyx (Malvaceae), including the description of six new species.” Systematic Botany, vol. 17, pp. 91-114, Jan. – Mar. 1992.

. J.F. Wendel and R.C. Cronn. “Polyploidy and the evolutionary history of cotton.” Adv Agron, vol. 78, pp. 139-186, 2003.

. J.F. Wendel, L.E. Flagel and K.L. Adams. “Jeans, Genes, and Genomes: Cotton as a Model for Studying Polyploidy.” in Polyploidy and Genome Evolution, P. S. Soltis and D. E. Soltis, Ed. Berlin, Germany: Springer, 2012, pp. 181-207.

. S.G. Stephens and M.E. Moseley. “Early Domesticated Cottons from Archaeological Sites in Central Coastal Peru.” Am Antiq, vol. 39, pp. 109-122, Jan. 1974.

. B.H. Zhang and R. Feng. Cotton resistance to insect and pest-resistant cotton. Beijing, China: Chinese Agricultural Science and Technology Press, 2000.

. A. Arpat, M. Waugh, J.P. Sullivan, M. Gonzales, D. Frisch, D. Main, T. Wood, A. Leslie, R. Wing and T. Wilkins. “Functional genomics of cell elongation in developing cotton fibers.” Plant Mol Biol, vol. 54, pp. 911-929, Apr. 2004.

. S. Samuel Yang, F. Cheung, J.J. Lee, M. Ha, N.E. Wei, S. Sze, D.M. Stelly, P. Thaxton, B. Triplett, C.D. Town and Z.J. Chen. “Accumulation of genome-specific transcripts, transcription factors and phytohormonal regulators during early stages of fiber cell development in allotetraploid cotton.” Plant J, vol. 47, pp. 761-775, Aug. 2006.

. Y.H. Shi, S.W. Zhu, X.Z. Mao, J.X. Feng, Y.M. Qin, L. Zhang, J. Cheng, L.P. Wei, Z.Y. Wang and Y.X. Zhu. “Transcriptome Profiling, Molecular Biological, and Physiological Studies Reveal a Major Role for Ethylene in Cotton Fiber Cell Elongation.” Plant Cell, vol. 18, pp. 651-664, Mar. 2006.

. J.A. Udall, J.M. Swanson, K. Haller, R.A. Rapp, M.E. Sparks, J. Hatfield, Y. Yu, Y. Wu, C. Dowd, A.B. Arpat, J.F. Wendel et al. “A global assembly of cotton ESTs.” Genome Res, vol. 16, pp. 441-450, Feb. 2006.

. Y. Wu, A.C. Machado, R.G. White, D.J. Llewellyn and E.S. Dennis. “Expression Profiling Identifies Genes Expressed Early During Lint Fibre Initiation in Cotton.” Plant Cell Physiol, vol. 47, pp. 107-127, Jan. 2006.

. X. Guan, N. Yu, X. Shangguan, S. Wang, S. Lu, L. Wang and X. Chen. “Arabidopsis trichome research sheds light on cotton fiber development mechanisms.” Chinese Sci Bull, vol. 52, pp. 1734-1741, Jul. 2007.

. S. Wang, J.W. Wang, N. Yu, C.H. Li, B. Luo, J.Y. Gou, L.J. Wang and X.Y. Chen. “Control of Plant Trichome Development by a Cotton Fiber MYB Gene.” Plant Cell, vol. 16, pp. 2323-2334, Sep. 2004.

. X. Guan, J.J. Lee, M. Pang, X. Shi, D.M. Stelly and Z.J. Chen. “Activation of Arabidopsis Seed Hair Development by Cotton Fiber-Related Genes.” PLoS ONE, vol.6, Jul. 2011.

. X. Guan, Q. Song and Z.J. Chen. “Polyploidy and small RNA regulation of cotton fiber development.” Trends Plant Sci, vol. 19, pp. 516-528, Aug. 2014.

. X.Y. Guan, Q.J. Li, C.M. Shan, S. Wang, Y.B. Mao, L.J. Wang and X.Y. Chen. “The HD-Zip IV gene GaHOX1 from cotton is a functional homologue of the Arabidopsis GLABRA2.” Physiol Plant vol. 134, pp. 174-182, Aug. 2008.

. G. Wang, G.H. Zhao, Y.H. Jia and X.M. Du. “Identification and Characterization of Cotton Genes Involved in Fuzz-Fiber Development.” J Integr Plant Biol, vol. 55, pp. 619-630, May 2013.

. J. Humphries, A. Walker, J. Timmis and S. Orford. “WD-repeat genes from cotton are functional homologues of the Arabidopsis thaliana TRANSPARENT TESTA GLABRA1 (TTG1) gene.” Plant Mol Biol, vol. 57, pp. 67-81, Jan. 2005.

. J.J. Esch, M. Chen, M. Sanders, M. Hillestad, S. Ndkium, B. Idelkope, J. Neizer and M.D. Marks. “A contradictory GLABRA3 allele helps define gene interactions controlling trichome development in Arabidopsis.” Development, vol. 130, pp. 5885-5894, 2003.

. X. Guan, M. Pang, G. Nah, X. Shi, W. Ye, D.M. Stelly and Z.J. Chen. “miR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development.” Nature, vol. 5, Jan. 2014.

. S.J. Clough and A.F. Bent. “Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.” Plant J, vol. 16, pp. 735-743, Oct. 1998.

. A. Junker, M.M. Muraya, K. Weigelt-Fischer, F. Arana-Ceballos, C. Klukas, A.E. Melchinger, R.C. Meyer, D. Riewe and T. Altmann. “Optimizing experimental procedures for quantitative evaluation of crop plant performance in high throughput phenotyping systems.” Front Plant Sci, vol. 5, Jan. 2015.

. J. Yuan, H. Yue, M. Zhang, J. Luo, L. Liu, W. Wu, T. Xiao, X. Chen, X. Chen, D. Zhang, R. Xing, X. Tong, N. Wu, J. Zhao, Y. Lu, M. Guo and R. Chen. “Transcriptional profiling analysis and functional prediction of long noncoding RNAs in cancer.” Oncotarget, vol. 7, pp. 8131–8142, Feb. 2016.

. K. Morohashi and E. Grotewold. “A Systems Approach Reveals Regulatory Circuitry for Arabidopsis Trichome Initiation by the GL3 and GL1 Selectors.” PLoS Genet, vol. 5, Feb. 2009.

Published
2019-12-16
Section
Articles