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Cotton ACAULIS5 is involved in stem elongation and the plant defense response to Verticillium dahliae through thermospermine alteration

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Abstract

Key message

Overexpression of GhACL5 , an ACAULIS5 from cotton, in Arabidopsis increased plant height and T-Spm level. Silencing of GhACL5 in cotton exhibited a dwarf phenotype and reduced resistance to Verticillium dahliae.

Abstract

The Arabidopsis thaliana gene ACAULIS5 (ACL5), for which inactivation causes a defect in stem elongation, encodes thermospermine (T-Spm) synthase. However, limited information is available about improvement in plant height by the overexpression of ACL5 gene, and the biological functions of ACL5 genes in response to biotic stress. Here, this study reports that constitutive expression of the cotton ACL5 gene (GhACL5) in Arabidopsis thaliana significantly increased plant height and elevated the level of T-Spm. Silencing of that gene in cotton reduced the amount of T-Spm and led to a severe dwarf phenotype. Expression of GhACL5 was induced upon treatment with the fungal pathogen Verticillium dahliae and plant hormones salicylic acid, jasmonic acid, and ethylene in resistant cotton plants, but gene silencing in cotton enhanced their susceptibility to V. dahliae infection. Furthermore, T-Spm exposure effectively inhibited V. dahliae growth in vitro. In summary, GhACL5 expression is related to in planta levels of T-Spm and is involved in stem elongation and defense responses against V. dahliae.

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Abbreviations

ACL5 :

ACAULIS5

Arg:

Arginine

ET:

Ethephon solution

GA:

Gibberellic acid

hpi:

Hours post-inoculation

HPLC:

High-performance liquid chromatography

JA:

Jasmonic acid

Orn:

Ornithine

PAs:

Polyamines

Put:

Putrescine

SA:

Salicylic acid

SAM:

S-Adenosylmethionine

SAMDC:

S-Adenosylmethionine decarboxylase

Spd:

Spermidine

Spm:

Spermine

SPMS:

Spm synthase

SSH:

Suppression subtractive hybridization

TRV:

Tobacco rattle virus

T-Spm:

Thermospermine

V. dahliae :

Verticillium dahliae

VIGS:

Virus-induced gene silencing

WT:

Wild-type

References

  • Akamatsu T, Hanzawa Y, Ohtake Y, Takahashi T, Nishitani K, Komeda Y (1999) Expression of endoxyloglucan transferase genes in acaulis mutants of Arabidopsis. Plant Physiol 121:715–722

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clay NK, Nelson T (2005) Arabidopsis thickvein mutation affects vein thickness and organ vascularization, and resides in a provascular cell-specific spermine synthase involved in vein definition and in polar auxin transport. Plant Physiol 138:767–777

    Article  PubMed Central  CAS  PubMed  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 

  • Dung JK, Hamm PB, Eggers JE, Johnson DA (2013) Incidence and impact of Verticillium dahliae in soil associated with certified potato seed lots. Phytopathology 103:55–63

    Article  PubMed  Google Scholar 

  • Gao X, Wheeler T, Li Z, Kenerley CM, He P, Shan L (2011) Silencing GhNDR1 and GhMKK2 compromises cotton resistance to Verticillium wilt. Plant J 66:293–305

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gonzalez ME, Marco F, Minguet EG, Carrasco-Sorli P, Blázquez MA, Carbonell J, Ruiz OA, Pieckenstain FL (2011) Perturbation of spermine synthase gene expression and transcript profiling provide new insights on the role of the tetraamine spermine in Arabidopsis defense against Pseudomonas viridiflava. Plant Physiol 156:2266–2277

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 19:4248–4256

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Imai A, Akiyama T, Kato T, Sato S, Tabata S, Yamamoto KT, Takahashi T (2004) Spermine is not essential for survival of Arabidopsis. FEBS Lett 556:148–152

    Article  CAS  PubMed  Google Scholar 

  • Imai A, Hanzawa Y, Komura M, Yamamoto KT, Komeda Y, Takahashi T (2006) The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene. Development 133:3575–3585

    Article  CAS  PubMed  Google Scholar 

  • Imai A, Komura M, Kawano E, Kuwashiro Y, Takahashi T (2008) A semi-dominant mutation in the ribosomal protein L10 gene suppresses the dwarf phenotype of the acl5 mutant in Arabidopsis thaliana. Plant J 56:881–890

    Article  CAS  PubMed  Google Scholar 

  • Kakehi J, Kuwashiro Y, Niitsu M, Takahashi T (2008) Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant Cell Physiol 49:1342–1349

    Article  CAS  PubMed  Google Scholar 

  • Kakehi J, Kuwashiro Y, Motose H, Igarashi K, Takahashi T (2010) Norspermine substitutes for thermospermine in the control of stem elongation in Arabidopsis thaliana. FEBS Lett 584:3042–3046

    Article  CAS  PubMed  Google Scholar 

  • Kakehi J, Kawano E, Yoshimoto K, Cai Q, Imai A, Takahashi T (2015) Mutations in ribosomal proteins, RPL4 and RACK1, suppress the phenotype of a thermospermine-deficient mutant of Arabidopsis thaliana. PLoS One 10(1):e0117309

    Article  PubMed Central  PubMed  Google Scholar 

  • Kim NH, Kim BS, Hwang BK (2013) Pepper arginine decarboxylase is required for polyamine and γ-aminobutyric acid signaling in cell death and defense response. Plant Physiol 162:2067–2083

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kim DW, Watanabe K, Murayama C, Izawa S, Niitsu M, Michael AJ, Berberich T, Kusano T (2014) Polyamine oxidase5 regulates Arabidopsis growth through thermospermine oxidase activity. Plant Physiol 165:1575–1590

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Knott JM, Römer P, Sumper M (2007) Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581:3081–3086

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luo J, Fuell C, Parr A, Hill L, Bailey P, Elliott K, Fairhurst SA, Martin C, Michael AJ (2009) A novel polyamine acyltransferase responsible for the accumulation of spermidine conjugates in Arabidopsis seed. Plant Cell 21:318–333

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mandal S, Mandal A, Johansson HE, Orjalo AV, Park MH (2013) Depletion of cellular polyamines, spermidine and spermine, causes a total arrest in translation and growth in mammalian cells. Proc Natl Acad Sci USA 110:2169–2174

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Marina M, Sirera FV, Rambla JL, Gonzalez ME, Blázquez MA, Carbonell J, Pieckenstain FL, Ruiz OA (2013) Thermospermine catabolism increases Arabidopsis thaliana resistance to Pseudomonas viridiflava. J Exp Bot 64:1393–1402

    Article  CAS  PubMed  Google Scholar 

  • Muñiz L, Minguet EG, Singh SK, Pesquet E, Vera-Sirera F, Moreau-Courtois CL, Carbonell J, Blázquez MA, Tuominen H (2008) ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development 135:2573–2582

    Article  PubMed  Google Scholar 

  • Nambeesan S, Abu Qamar S, Laluk K, Mattoo AK, Mickelbart MV, Ferruzzi MG, Mengiste T, Handa AK (2012) Polyamines attenuate ethylene-mediated defense responses to abrogate resistance to Botrytis cinerea in tomato. Plant Physiol 158:1034–1045

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oshima T (1979) A new polyamine, thermospermine, 1,12-diamino-4,8-diazadodecane, from an extreme thermophile. J Biol Chem 254:8720–8722

    CAS  PubMed  Google Scholar 

  • Wu LZ, Wang XF, Zhang Y, Li XH, Zhang GY, Wu LQ, Li ZK, Ma ZY (2014) Function of acid insoluble lignin and GhLaccase in cotton resistance to Verticillium wilt. Acta Agron Sin 40:1157–1163

    CAS  Google Scholar 

  • Xu F, Yang L, Zhang J, Guo X, Zhang X, Li G (2012) Prevalence of the defoliating pathotype of Verticillium dahliae on cotton in central China and virulence on selected cotton cultivars. J Phytopathol 160:369–376

    Article  Google Scholar 

  • Zhang CY, Wang XF, Zhang GY, Wu LQ, Chi JN, Li ZK, Ma ZY (2010) ESTs analysis of suppression subtractive hybridization library from upland cotton resistant cultivar infected by Verticillium dahliae. Cotton Sci 22:17–22

    CAS  Google Scholar 

  • Zhang Y, Wang XF, Yang S, Chi JN, Zhang GY, Ma ZY (2011) Cloning and characterization of a Verticillium wilt resistance gene from Gossypium barbadense and functional analysis in Arabidopsis thaliana. Plant Cell Rep 30:2085–2096

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Wang XF, Ding ZG, Ma Q, Zhang GR, Zhang SL, Li ZK, Wu LQ, Zhang GY, Ma ZY (2013) Transcriptome profiling of Gossypium barbadense inoculated with Verticillium dahliae provides a resource for cotton improvement. BMC Genom 14:637

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the 863 Project of China (No. 2013AA102601-5) and the Science & Technology Pillar Program of Hebei Province (14226308D). We are grateful to Priscilla Licht for critical reading of the manuscript. We thank Yule Liu of Tsinghua University for kindly offering the TRV vector, and Sun Yan-xiang of Langfang Normal University for kindly offering the pGN vector.

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Correspondence to Zhiying Ma.

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Communicated by P. Lakshmanan.

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Mo, H., Wang, X., Zhang, Y. et al. Cotton ACAULIS5 is involved in stem elongation and the plant defense response to Verticillium dahliae through thermospermine alteration. Plant Cell Rep 34, 1975–1985 (2015). https://doi.org/10.1007/s00299-015-1844-3

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