Plant Cell Reports

, Volume 34, Issue 11, pp 1975–1985 | Cite as

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

  • Huijuan Mo
  • Xingfen Wang
  • Yan Zhang
  • Jun Yang
  • Zhiying Ma
Original Article

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.

Keywords

ACAULIS5 Thermospermine Stem elongation Cotton Arabidopsis thaliana Verticillium dahliae 

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

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 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 121:715–722PubMedCentralCrossRefPubMedGoogle Scholar
  2. 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 138:767–777PubMedCentralCrossRefPubMedGoogle Scholar
  3. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  4. Dung JK, Hamm PB, Eggers JE, Johnson DA (2013) Incidence and impact of Verticillium dahliae in soil associated with certified potato seed lots. Phytopathology 103:55–63CrossRefPubMedGoogle Scholar
  5. 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 66:293–305PubMedCentralCrossRefPubMedGoogle Scholar
  6. 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 156:2266–2277PubMedCentralCrossRefPubMedGoogle Scholar
  7. 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 19:4248–4256PubMedCentralCrossRefPubMedGoogle Scholar
  8. 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 556:148–152CrossRefPubMedGoogle Scholar
  9. 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 133:3575–3585CrossRefPubMedGoogle Scholar
  10. 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 56:881–890CrossRefPubMedGoogle Scholar
  11. Kakehi J, Kuwashiro Y, Niitsu M, Takahashi T (2008) Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant Cell Physiol 49:1342–1349CrossRefPubMedGoogle Scholar
  12. 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 584:3042–3046CrossRefPubMedGoogle Scholar
  13. 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):e0117309PubMedCentralCrossRefPubMedGoogle Scholar
  14. 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 162:2067–2083PubMedCentralCrossRefPubMedGoogle Scholar
  15. 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 165:1575–1590PubMedCentralCrossRefPubMedGoogle Scholar
  16. Knott JM, Römer P, Sumper M (2007) Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581:3081–3086CrossRefPubMedGoogle Scholar
  17. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta C(T)) method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  18. 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 21:318–333PubMedCentralCrossRefPubMedGoogle Scholar
  19. 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 110:2169–2174PubMedCentralCrossRefPubMedGoogle Scholar
  20. 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 64:1393–1402CrossRefPubMedGoogle Scholar
  21. 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 135:2573–2582CrossRefPubMedGoogle Scholar
  22. 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 158:1034–1045PubMedCentralCrossRefPubMedGoogle Scholar
  23. Oshima T (1979) A new polyamine, thermospermine, 1,12-diamino-4,8-diazadodecane, from an extreme thermophile. J Biol Chem 254:8720–8722PubMedGoogle Scholar
  24. 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 40:1157–1163Google Scholar
  25. 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 160:369–376CrossRefGoogle Scholar
  26. 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 22:17–22Google Scholar
  27. 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 30:2085–2096CrossRefPubMedGoogle Scholar
  28. 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 14:637CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Huijuan Mo
    • 1
  • Xingfen Wang
    • 1
  • Yan Zhang
    • 1
  • Jun Yang
    • 1
  • Zhiying Ma
    • 1
  1. 1.North China Key Laboratory for Germplasm Resources of Education MinistryHebei Agricultural UniversityBaodingChina

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