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Role of a cotton endoreduplication-related gene, GaTOP6B, in response to drought stress

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Abstract

Main conclusion

Cotton GaTOP6B is involved in cellular endoreduplication and a positive response to drought stress via promoting plant leaf and root growth.

Drought is deemed as one of adverse conditions that could cause substantial reductions in crop yields worldwide. Since cotton exhibits a moderate-tolerant phenotype under water-deficit conditions, the plant could therefore be used to characterize potential new genes regulating drought tolerance in crop plants. In this work, GaTOP6B, encoding DNA topoisomerase VI subunit B, was identified in Asian cotton (Gossypium arboreum). Virus-induced gene silencing (VIGS) and overexpression (OE) were used to investigate the biological function of GaTOP6B in G. arboreum and Arabidopsis thaliana under drought stress. The GaTOP6B-silencing plants showed a reduced ploidy level, and displayed a compromised tolerance phenotype including lowered relative water content (RWC), decreased proline content and antioxidative enzyme activity, and an increased malondialdehyde (MDA) content under drought stress. GaTOP6B-overexpressing Arabidopsis lines, however, had increased ploidy levels, and were more tolerant to drought treatment, associated with improved RWC maintenance, higher proline accumulation, and reduced stomatal aperture under drought stress. Transcriptome analysis showed that genes involved in the processes like cell cycle, transcription and signal transduction, were substantially up-regulated in GaTOP6B-overexpressing Arabidopsis, promoting plant growth and development. More specifically, under drought stress, the genes involved in the biosynthesis of secondary metabolites such as phenylpropanoid, starch and sucrose were selectively enhanced to improve tolerance in plants. Taken together, the results demonstrated that GaTOP6B could coordinately regulate plant leaf and root growth via cellular endoreduplication, and positively respond to drought stress. Thus, GaTOP6B could be a competent candidate gene for improvement of drought tolerance in crop species.

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Abbreviations

DEG:

Differentially expressed genes

ORF:

Open reading frame

RWC:

Relative water content

TOP6B:

Topoisomerase VIB

VIGS:

Virus-induced gene silencing

References

  • An XJ, Deng ZY, Wang T (2011) OsSpo11-4, a rice homologue of the archaeal TopVIA protein, mediates double-strand DNA cleavage and interacts with OsTopVIB. PLoS One 6:e20327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386:414–417

    Article  CAS  PubMed  Google Scholar 

  • Blattner FR (2015) TOPO6: a nuclear single-copy gene for plant phylogenetic inference. Plant Syst Evol 302:239–244

    Article  Google Scholar 

  • Breuer C, Stacey NJ, West CE, Zhao Y, Chory J, Tsukaya H, Azumi Y, Maxwell A, Roberts K, Sugimoto-Shirasu K (2007) BIN4, a novel component of the plant DNA topoisomerase VI complex, is required for endoreduplication in Arabidopsis. Plant Cell 19:3655–3668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breuer C, Braidwood L, Sugimoto K (2014) Endocycling in the path of plant development. Curr Opin Plant Biol 17:78–85

    Article  CAS  PubMed  Google Scholar 

  • Butt HI, Yang Z, Chen E, Zhao G, Gong Q, Yang Z, Zhang X, Li F (2017) Functional characterization of cotton GaMYB62L, a novel R2R3 TF in transgenic Arabidopsis. PLoS One 12:e0170578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ceccarelli M, Santantonio E, Marmottini F, Amzallag GN, Cionini PG (2006) Chromosome endoreduplication as a factor of salt adaptation in Sorghum bicolor. Protoplasma 227:113–118

    Article  CAS  PubMed  Google Scholar 

  • Chen T, Li W, Hu X, Guo J, Liu A, Zhang B (2015) A cotton MYB transcription factor, GbMYB5, is positively involved in plant adaptive response to drought stress. Plant Cell Physiol 56:917–929

    Article  CAS  PubMed  Google Scholar 

  • Cheng XQ, Zhu XF, Tian WG, Cheng WH, Hakim Sun J, Jin SX, Zhu HG (2017) Genome-wide identification and expression analysis of polyamine oxidase genes in upland cotton (Gossypium hirsutum L.). Plant Cell Tiss Organ Cult 129:237–249

    Article  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Corbett KD, Berger JM (2003) Structure of the topoisomerase VI-B subunit: implications for type II topoisomerase mechanism and evolution. EMBO J 22:151–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Veylder L, Larkin JC, Schnittger A (2011) Molecular control and function of endoreplication in development and physiology. Trends Plant Sci 16:624–634

    Article  CAS  PubMed  Google Scholar 

  • Eady C, Weld R, Lister C (2000) Agrobacterium tumefaciens-mediated transformation and transgenic-plant regeneration of onion (Allium cepa L.). Plant Cell Rep 19:376–381

    Article  CAS  PubMed  Google Scholar 

  • Elmaghrabi AM, Rogers HJ, Francis D, Ochatt S (2017) PEG induces high expression of the cell cycle checkpoint gene WEE1 in embryogenic callus of Medicago truncatula: potential link between cell cycle checkpoint regulation and drought. Front Plant Sci 8:1479

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao X, Shan L (2013) Functional genomic analysis of cotton genes with Agrobacterium-mediated virus-induced gene silencing. Methods Mol Biol 975:157–165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gegas VC, Wargent JJ, Pesquet E, Granqvist E, Paul ND, Doonan JH (2014) Endopolyploidy as a potential alternative adaptive strategy for Arabidopsis leaf size variation in response to UV-B. J Exp Bot 65:2757–2766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartung F, Puchta H (2001) Molecular characterization of homologues of both subunits A (SPO11) and B of the archaebacterial topoisomerase 6 in plants. Gene 271:81–86

    Article  CAS  PubMed  Google Scholar 

  • Hartung F, Angelis KJ, Meister A, Schubert I, Melzer M, Puchta H (2002) An archaebacterial topoisomerase homolog not present in other eukaryotes is indispensable for cell proliferation of plants. Curr Biol 12:1787–1791

    Article  CAS  PubMed  Google Scholar 

  • Hase Y, Trung KH, Matsunaga T, Tanaka A (2006) A mutation in the uvi4 gene promotes progression of endo-reduplication and confers increased tolerance towards ultraviolet B light. Plant J 46:317–326

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Tyagi AK, Khurana JP (2006) Overexpression of putative topoisomerase 6 genes from rice confers stress tolerance in transgenic Arabidopsis plants. FEBS J 273:5245–5260

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Tyagi AK, Khurana JP (2008) Constitutive expression of a meiotic recombination protein gene homolog, OsTOP6A1, from rice confers abiotic stress tolerance in transgenic Arabidopsis plants. Plant Cell Rep 27:767–778

    Article  CAS  PubMed  Google Scholar 

  • Kirik V, Schrader A, Uhrig JF, Hülskamp M (2007) MIDGET unravels functions of the Arabidopsis topoisomerase VI complex in DNA endoreduplication, chromatin condensation, and transcriptional silencing. Plant Cell 19:3100–3110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leclercq J, Martin F, Sanier C, Clement-Vidal A, Fabre D, Oliver G, Lardet L, Ayar A, Peyramard M, Montoro P (2012) Over-expression of a cytosolic isoform of the HbCuZnSOD gene in Hevea brasiliensis changes its response to a water deficit. Plant Mol Biol 80:255–272

    Article  CAS  PubMed  Google Scholar 

  • Lefebvre V, North H, Frey A, Sotta B, Seo M, Okamoto M, Nambara E, Marion-Poll A (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J 45:309–319

    Article  CAS  PubMed  Google Scholar 

  • Lopienska-Biernat E, Molcan T, Paukszto L, Jastrzebski JP, Myszczynski K (2018) Modelling studies determining the mode of action of anthelmintics inhibiting in vitro trehalose-6-phosphate phosphatase (TPP) of Anisakis simplex s.l. Exp Parasitol 184:46–56

    Article  CAS  PubMed  Google Scholar 

  • Lubbers EL, Chee PW, Saranga Y, Paterson AH (2007) Recent advances and future prospective in molecular breeding of cotton for drought and salinity stress tolerance. In: Jenks MA, Hasegawa PM, Jain SM (eds) Advances in molecular breeding towards drought and salt tolerant crops. Springer, Dordrecht, pp 775–796

    Chapter  Google Scholar 

  • Ma LF, Li Y, Chen Y, Li XB (2016) Improved drought and salt tolerance of Arabidopsis thaliana by ectopic expression of a cotton (Gossypium hirsutum) CBF gene. Plant Cell Tiss Organ Cult 124:583–598

    Article  CAS  Google Scholar 

  • Miao BH, Han XG, Zhang WH (2010) The ameliorative effect of silicon on soybean seedlings grown in potassium-deficient medium. Ann Bot 105:967–973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mustafa R, Shafiq M, Mansoor S, Briddon RW, Scheffler BE, Scheffler J, Amin I (2016) Virus-induced gene silencing in cultivated cotton (Gossypium spp.) using tobacco rattle virus. Mol Biotechnol 58:65–72

    Article  CAS  PubMed  Google Scholar 

  • Nir I, Shohat H, Panizel I, Olszewski N, Aharoni A, Weiss D (2017) The tomato DELLA protein PROCERA acts in guard cells to promote stomatal closure. Plant Cell 29:3186–3197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pirrello J, Deluche C, Frangne N, Gevaudant F, Maza E, Djari A, Bourge M, Renaudin JP, Brown S, Bowler C, Zouine M, Chevalier C, Gonzalez N (2018) Transcriptome profiling of sorted endoreduplicated nuclei from tomato fruits: how the global shift in expression ascribed to DNA ploidy influences RNA-Seq data normalization and interpretation. Plant J 93:387–398

    Article  CAS  PubMed  Google Scholar 

  • Radziejwoski A, Vlieghe K, Lammens T, Berckmans B, Maes S, Jansen MA, Knappe C, Albert A, Seidlitz HK, Bahnweg G, Inze D, De Veylder L (2011) Atypical E2F activity coordinates PHR1 photolyase gene transcription with endoreduplication onset. EMBO J 30:355–363

    Article  CAS  PubMed  Google Scholar 

  • Saleem MF, Sammar Raza MA, Ahmad S, Khan IH, Shahid AM (2016) Understanding and mitigating the impacts of drought stress in cotton—a review. Pak J Agric Sci 53:609–623

    Google Scholar 

  • Scholes DR, Paige KN (2015) Plasticity in ploidy: a generalized response to stress. Trends Plant Sci 20:165–175

    Article  CAS  PubMed  Google Scholar 

  • Sekmen AH, Ozgur R, Uzilday B, Turkan I (2014) Reactive oxygen species scavenging capacities of cotton (Gossypium hirsutum) cultivars under combined drought and heat induced oxidative stress. Environ Exp Bot 99:141–149

    Article  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto-Shirasu K, Stacey NJ, Corsar J, Roberts K, McCann MC (2002) DNA topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr Biol 12:1782–1786

    Article  CAS  PubMed  Google Scholar 

  • Villeneuve AM, Hillers KJ (2001) Whence meiosis. Cell 106:647–650

    Article  CAS  PubMed  Google Scholar 

  • Wang NN, Zhao LL, Lu R, Li Y, Li XB (2015) Cotton mitogen-activated protein kinase4 (GhMPK4) confers the transgenic Arabidopsis hypersensitivity to salt and osmotic stresses. Plant Cell Tiss Organ Cult 123:619–632

    Article  CAS  Google Scholar 

  • Woolfenden HC, Bourdais G, Kopischke M, Miedes E, Molina A, Robatzek S, Morris RJ (2017) A computational approach for inferring the cell wall properties that govern guard cell dynamics. Plant J 92:5–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin Y, Cheong H, Friedrichsen D, Zhao Y, Hu J, Mora-Garcia S, Chory J (2002) A crucial role for the putative Arabidopsis topoisomerase VI in plant growth and development. Proc Natl Acad Sci USA 99:10191–10196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao F, Ma J, Li L, Fan S, Guo Y, Song M, Wei H, Pang C, Yu S (2016) GhNAC12, a neutral candidate gene, leads to early aging in cotton (Gossypium hirsutum L.). Gene 576:268–274

    Article  CAS  PubMed  Google Scholar 

  • Zhou L, Wang NN, Kong L, Gong SY, Li Y, Li XB (2014) Molecular characterization of 26 cotton WRKY genes that are expressed differentially in tissues and are induced in seedlings under high salinity and osmotic stress. Plant Cell Tiss Organ Cult 119:141–153

    Article  CAS  Google Scholar 

  • Zhou L, Wang NN, Gong SY, Lu R, Li Y, Li XB (2015) Overexpression of a cotton (Gossypium hirsutum) WRKY gene, GhWRKY34, in Arabidopsis enhances salt-tolerance of the transgenic plants. Plant Physiol Biochem 96:311–320

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was financially supported by the Program for Science and Technology Innovation Talents in Universities of Henan Province (No. 19HASTIT014), and the National Natural Science Foundation of China (No. 31600995) and the fund of the Science and Technology Cooperation Projects of Henan Province of China (No. 152106000055).

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Correspondence to Fang Wei, Baoming Tian or Jinyong Huang.

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The experiments in this study comply with the current laws of China.

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Electronic supplementary material

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Supplementary material 1 Bioinformatic analysis of GaTOP6B (JPEG 149 kb)

Supplementary material 2 Subcellular localization of GaTOP6B (JPEG 16 kb)

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Supplementary material 3 Characterization of CLA-silencing plantlets and GaTOP6B-overexpressing Arabidopsis (JPEG 36 kb)

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Supplementary material 4 Survival rate and DAB staining and chlorophyll content in GaTOP6B-silencing cotton under drought stress (JPEG 57 kb)

Supplementary material 5 Gene expression analysis (JPEG 209 kb)

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Supplementary material 6 COG classification of DEGs in transgenic Arabidopsis compared to WT under 200 mM mannitol treatment (JPEG 57 kb)

Supplementary material 7 (JPEG 62 kb)

Supplementary material 8 (DOC 42 kb)

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Tian, Y., Gu, H., Fan, Z. et al. Role of a cotton endoreduplication-related gene, GaTOP6B, in response to drought stress. Planta 249, 1119–1132 (2019). https://doi.org/10.1007/s00425-018-3067-7

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