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Breadfruit (Artocarpus altilis) DELLA genes: gibberellin-regulated stem elongation and response to high salinity and drought

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Abstract

Breadfruit (Artocarpus altilis) is a traditional staple tree crop in the Oceania. Susceptibility to tropical windstorm damage has driven an interest in developing breadfruit with dwarf stature. Gibberellin (GA) is one of the most important determinants of plant height and DELLA proteins are repressors of GA signalling pathway. As a first step toward understanding the molecular mechanism of growth regulation in the species, we isolated two full-length DELLA cDNAs, AaDELLA1 and AaDELLA2 from breadfruit. Sequence analysis indicated the deduced proteins encoded by these AaDELLAs bear all the hallmarks of functional DELLA of other species. Transcripts of AaDELLA1 and AaDELLA2 were detected in all plant organs, but the expression was much lower in flowers and fruits. AaDELLA1 showed predominantly higher expression in roots, but AaDELLA2 displayed higher expression in stems and leaves. Expression of both AaDELLAs was not significantly changed by exogenous GA3 treatment. Under paclobutrazol treatment, the expression of AaDELLA2 was up-regulated, but the expression of AaDELLA1 was not changed significantly. Treatments of high salinity up-regulated the expression levels of both AaDELLA1 and AaDELLA2. Treatment of drought stress increased the expression of AaDELLA2, but not that of AaDELLA1. The function of AaDELLAs is discussed with particular reference to their role in stem elongation and the opportunities of breadfruit dwarfing.

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References

  • Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20:2117–2129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An J, Hou L, Li C, Wang CX, Xia H, Zhao CZ, Li CS, Zheng YX, Zhao YX, Wang X (2015) Cloning and expression analysis of four DELLA genes in peanut. Russ J Plant Physiol 62:116–126

    Article  CAS  Google Scholar 

  • Bassel GW, Zielinska E, Mullen RT, Bewley JD (2004) Down-regulation of DELLA genes is not essential for germination of tomato, soybean, and Arabidopsis seeds. Plant Physiol 136:2782–2789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Best NB, Wang XG, Brittsan S, Dean E, Helfers SJ, Homburg R, Mobley ML, Spindler TL, Xie BF, Zhang ML, Hasegawa PM, Joly RJ, Rhodes D, Dilkes BP (2016) Sunflower ‘sunspot’ is hyposensitive to GA(3) and has a missense mutation in the DELLA motif of HaDella1. J Am Soc Hortic Sci 141:389–394

    Google Scholar 

  • Boss PK, Thomas MR (2002) Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature 416:847–850

    Article  CAS  PubMed  Google Scholar 

  • Chandler PM, Marion-Poll A, Ellis M FG (2002) Mutants at the slender1 locus of barley cv himalaya: molecular and physiological characterization. Plant Physiol 129:181–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colebrook E, Thomas S, Phillips A, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217:67–75

    Article  CAS  PubMed  Google Scholar 

  • Floss DS, Levy JG, Lévesque-Tremblay V, Pumplin N, Harrison MJ (2013) DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc Nat Acad Sci USA 110:E5025–E5034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foster T, Kirk C, Jones WT, Allan AC, Espley R, Karunairetnam S, Rakonjac J (2007) Characterisation of the DELLA subfamily in apple (Malus x domestica Borkh.). Tree Genetics Genomes 3:187–197

    Article  Google Scholar 

  • Gao Y, Li TT, Liu Y, Ren CX, Zhao Y, Wang ML (2010) Isolation and characterization of gene encoding G protein alpha subunit protein responsive to plant hormones and abiotic stresses in Brassica napus. Mol Biol Rep 37:3957–3965

    Article  CAS  PubMed  Google Scholar 

  • Gao SJ, Xie XZ, Yang SG, Chen ZP, Wang XJ (2012a) The changes of GA level and signaling are involved in the regulation of mesocotyl elongation during blue light mediated de-etiolation in Sorghum bicolor. Mol Biol Rep 39:4091–4100

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Chen JM, Zhao Y, Li TT, Wang ML (2012b) Molecular cloning and expression analysis of a RGA-like gene responsive to plant hormones in Brassica napus. Mol Biol Rep 39:1957–1962

    Article  CAS  PubMed  Google Scholar 

  • Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151

    Article  PubMed  PubMed Central  Google Scholar 

  • Grimplet J, Agudelo-Romero P, Teixeira RT, Martinez-Zapater JM, Fortes AM (2016) Structural and functional analysis of the GRAS gene family in grapevine indicates a role of GRAS proteins in the control of development and stress responses. Front Plant Sci 7:353

    Article  PubMed  PubMed Central  Google Scholar 

  • Hedden P, Phillips A (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Gao YR, Wei W, Zhang K, Feng JY (2016) Strawberry MOTHER OF FT AND TFL1 regulates seed germination and post-germination growth through integrating GA and ABA signaling in Arabidopsis. Plant Cell Tissue Organ Cult 126:343–352

    Article  CAS  Google Scholar 

  • Knight H, Knight M (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267

    Article  CAS  PubMed  Google Scholar 

  • Lawit SJ, Wych HM, Xu D, Kundu S, Tomes DT (2010) Maize DELLA proteins dwarf plant8 and dwarf plant9 as modulators of plant development. Plant Cell Physiol 51:1854–1868

    Article  CAS  PubMed  Google Scholar 

  • Liao WB, Ruan MB, Cui BM, Xu NF, Lu JJ, Peng M (2009) Isolation and characterization of a GAI/RGA-like gene from Gossypium hirsutum. Plant Growth Regul 58:35–45

    Article  CAS  Google Scholar 

  • Liu C, Wang JL, Huang TD, Wang F, Yuan F, Cheng XM, Zhang Y, Shi SW, Wu JS, Liu KD (2010) A missense mutation in the VHYNP motif of a DELLA protein causes a semi-dwarf mutant phenotype in Brassica napus. Theor Appl Genet 121:249–258

    Article  CAS  PubMed  Google Scholar 

  • Liu TM, Zhu SY, Tang QM, Yu YT, Tang SW (2013) Identification of drought stress-responsive transcription factors in ramie (Boehmeria nivea L. Gaud). BMC Plant Biol 13:130–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Xuan L, Xu L-A, Huang M, Xu M (2016) Molecular cloning, expression analysis and subcellular localization of four DELLA genes from hybrid poplar. SpringerPlus 5:1129

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo J, Ma N, Pei HX, Chen JW, Li J, Gao JP (2013) A DELLA gene, RhGAI1, is a direct target of EIN3 and mediates ethylene-regulated rose petal cell expansion via repressing the expression of RhCesA2. J Exp Bot 64:5075–5084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J 56:613–626

    Article  CAS  PubMed  Google Scholar 

  • Muangprom A, Thomas SG, Sun TP, Osborn TC (2005) A novel dwarfing mutation in a green revolution gene from Brassica rapa. Plant Physiol 137:931–938. doi:10.1104/pp.104.057646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mutasa-Gottgens E, Hedden P (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 60:1979–1989. doi:10.1093/jxb/erp040

    Article  PubMed  Google Scholar 

  • Niu SH, Gao Q, Li ZX, Chen XY, Li W (2014) The role of gibberellin in the CBF1-mediated stress-response pathway. Plant Mol Biol Rep 32:852–863

    Article  CAS  Google Scholar 

  • Ogawa M, Kusanoa T, Katsumib M, Sano H (2000) Rice gibberellin insensitive gene homolog, OsGAI, encodes a nuclear-localized protein capable of gene activation at transcriptional level. Gene 245:21–29

    Article  CAS  PubMed  Google Scholar 

  • Oki LR, Lieth JH (2004) Effect of changes in substrate salinity on the elongation of Rosa hybrida L. ‘Kardinal’ stems. Sci Hortic 101:103–119

    Article  CAS  Google Scholar 

  • Olszewski N, Sun TP, Gubler F (2002) Gibberellin signalling, biosynthesis, catabolism, and response pathways. Plant Cell 14:S61–S80

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peng J, Richards D, Hartley N, Murphy G, Devos K, Flintham J, Beales J, Fish L, Worland A, Pelica F, Sudhaka D, Christou P, Snape J, Gale M, Harberd N (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261

    Article  CAS  PubMed  Google Scholar 

  • Ragone D (1997) Breadfruit, Artocarpus altilis (Parkinson) Fosberg. Promoting the conservation and use of underutilized and neglected crops. 10. Gatersleben/International Plant Genetic Resources Institute, Rome

    Google Scholar 

  • Sakata T, Oda S, Tsunaga Y, Shomura H, Kawagishi-Kobayashi M, Aya K, Saeki K, Endo T, Nagano K, Kojima M, Sakakibara H, Watanabe M, Matsuoka M, Higashitani A (2014) Reduction of gibberellin by low temperature disrupts pollen development in rice. Plant Physiol 164:2011–2019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sawada Y, Umetsu A, Komatsu Y, Kitamura J, Suzuki H, Asami T, Fukuda M, Honda I, Mitsuhashi W, Nakajima M, Toyomasu T (2012) An unusual spliced variant of DELLA protein, a negative regulator of gibberellin signalin, in lettuce. Biosci Biotechnol Biochem 76:544–550

    Article  CAS  PubMed  Google Scholar 

  • Silverstone AL, Jung HS, Dill A, Kawaide H, Kamiya Y, T.p. Sun (2001) Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13:1555–1566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun T, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55:197–223

    Article  CAS  PubMed  Google Scholar 

  • Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun T-p (2004) DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wahome PK, Jesch HH, Grittner I (2000) Effect of NaCl on the vegetative growth and flower quality of roses. J Appl Bot 74:38–41

    Google Scholar 

  • Wang SS, Sun C, Liu ZZ, Shi QH, Yao YX, You CX, Hao YJ (2012) Ectopic expression of the apple mhgai2 gene brings about GA-insensitive phenotypes in tomatoes. Acta Physiol Plant 34:2369–2377

    Article  CAS  Google Scholar 

  • Wang G-L, Que F, Xu Z-S, Wang F, Xiong A-S (2015) Exogenous gibberellin altered morphology, anatomic and transcriptional regulatory networks of hormones in carrot root and shoot. BMC Plant Biol 15:290

    Article  PubMed  PubMed Central  Google Scholar 

  • Wen W, Cui B, Yu X, Chen Q, Zheng Y, Xia Y, Peng M (2012) Functional analysis of cotton DELLA-Like genes that are differentially regulated during fiber development. Plant Mol Biol Rep 30:1014–1024

    Article  CAS  Google Scholar 

  • Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EMN, Maier A, Schwechheimer C (2007) The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 19:1209–1220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zawaski C, Busov VB (2014) Roles of gibberellin catabolism and signaling in growth and physiological response to drought and short-day photoperiods in populus trees. PLoS ONE 9:e86217

    Article  PubMed  PubMed Central  Google Scholar 

  • Zerega N, Ragone D, Motley TJ (2004) Complex origins of breadfruit (Artocarpus altilis, Moraceae): implications for human migrations in Oceania. Am J Bot 91:760–766

    Article  PubMed  Google Scholar 

  • Zhou Y, Underhill S (2015) Breadfruit (Artocarpus altilis) gibberellin 20-oxidase genes: sequence variants, stem elongation and abiotic stress response. Tree Genet Genomes 11:1–13

    Article  CAS  Google Scholar 

  • Zhou Y, Underhill S (2016) Breadfruit (Artocarpus altilis) gibberellin 2-oxidase genes in stem elongation and abiotic stress response. Plant Physiol Biochem 98:81–88

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Andriunas F, Offler CE, McCurdy DW, Patrick JW (2010) An epidermal-specific ethylene signal cascade regulates trans-differentiation of transfer cells in Vicia faba cotyledons. New Phytol 185:931–943

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Taylor MB, Underhill SJR (2014) Dwarfing of breadfruit (Artocarpus altilis) trees: opportunities and challenges. Am J Exp Agric 4:1743–1763

    Article  Google Scholar 

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Acknowledgements

This work was funded by the Australia Centre for International Agriculture Research (ACIAR) through project HORT 2014-077.

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Authors and Affiliations

  1. Faculty of Science, Education and Engineering, University of the Sunshine Coast, Sippy Downs, QLD, 4556, Australia

    Yuchan Zhou & Steven J. R. Underhill

  2. Queensland Alliance for Agriculture and Food Innovation, University of Queensland, St Lucia, QLD, 4072, Australia

    Yuchan Zhou & Steven J. R. Underhill

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  1. Yuchan Zhou
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Correspondence to Yuchan Zhou.

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Zhou, Y., Underhill, S.J.R. Breadfruit (Artocarpus altilis) DELLA genes: gibberellin-regulated stem elongation and response to high salinity and drought. Plant Growth Regul 83, 375–383 (2017). https://doi.org/10.1007/s10725-017-0302-3

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  • DOI: https://doi.org/10.1007/s10725-017-0302-3

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