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Title: Molecular cloning of the tomato Hairless gene implicates actin dynamics in trichome-mediated defense and mechanical properties of stem tissue

Abstract

Abstract Trichomes are epidermal structures that provide a first line of defense against arthropod herbivores. The recessive hairless (hl) mutation in tomato (Solanum lycopersicum L.) causes severe distortion of trichomes on all aerial tissues, impairs the accumulation of sesquiterpene and polyphenolic compounds in glandular trichomes, and compromises resistance to the specialist herbivore Manduca sexta. Here, we demonstrate that the tomato Hl gene encodes a subunit (SRA1) of the highly conserved WAVE regulatory complex that controls nucleation of actin filaments in a wide range of eukaryotic cells. The tomato SRA1 gene spans a 42-kb region containing both Solyc11g013280 and Solyc11g013290. The hl mutation corresponds to a complex 3-kb deletion that removes the last exon of the gene. Expression of a wild-type SRA1 cDNA in the hl mutant background restored normal trichome development, accumulation of glandular trichome-derived metabolites, and resistance to insect herbivory. These findings establish a role for SRA1 in the development of tomato trichomes and also implicate the actin-cytoskeleton network in cytosolic control of specialized metabolism for plant defense. We also show that the brittleness of hl mutant stems is associated with altered mechanical and cell morphological properties of stem tissue, and demonstrate that this defect is directly linked tomore » the mutation in SRA1.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [4];  [3]; ORCiD logo [6];  [7]
  1. Department of Energy-Plant Research Laboratory, Michigan State University, East Lansing, MI, USA, Graduate School of International Agricultural Technology and Crop Biotechnology Institute/GreenBio Science and Technology, Seoul National University, Pyeongchang, Republic of Korea
  2. Department of Energy-Plant Research Laboratory, Michigan State University, East Lansing, MI, USA
  3. Department of Energy-Plant Research Laboratory, Michigan State University, East Lansing, MI, USA, Department of Plant Biology, Michigan State University, East Lansing, MI, USA
  4. Department of Plant Biology, Michigan State University, East Lansing, MI, USA
  5. Department of Chemistry, Michigan State University, East Lansing, MI, USA, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, USA
  6. Department of Energy-Plant Research Laboratory, Michigan State University, East Lansing, MI, USA, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, USA
  7. University of Essex
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States); Univ. of California, Davis, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division; USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Science Foundation (NSF); Organisation for Economic Co-operation and Development (OECD); Rural Development Administration (Korea, Republic of)
OSTI Identifier:
1608739
Alternate Identifier(s):
OSTI ID: 1427733
Grant/Contract Number:  
FC02-07ER64494; FG02-91ER20021; DBI-0604336; IOS-1456864
Resource Type:
Published Article
Journal Name:
Journal of Experimental Botany
Additional Journal Information:
Journal Name: Journal of Experimental Botany Journal Volume: 67 Journal Issue: 18; Journal ID: ISSN 0022-0957
Publisher:
Oxford University Press
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Actin-cytoskeleton network; cell wall; mechanical properties; plant-insect interaction; specialized metabolism; terpenoid; tomato (Solanum lycopersicum); trichome

Citation Formats

Kang, Jin-Ho, Campos, Marcelo L., Zemelis-Durfee, Starla, Al-Haddad, Jameel M., Jones, A. Daniel, Telewski, Frank W., Brandizzi, Federica, Howe, Gregg A., and Raines, ed., Christine. Molecular cloning of the tomato Hairless gene implicates actin dynamics in trichome-mediated defense and mechanical properties of stem tissue. United Kingdom: N. p., 2016. Web. doi:10.1093/jxb/erw292.
Kang, Jin-Ho, Campos, Marcelo L., Zemelis-Durfee, Starla, Al-Haddad, Jameel M., Jones, A. Daniel, Telewski, Frank W., Brandizzi, Federica, Howe, Gregg A., & Raines, ed., Christine. Molecular cloning of the tomato Hairless gene implicates actin dynamics in trichome-mediated defense and mechanical properties of stem tissue. United Kingdom. doi:10.1093/jxb/erw292.
Kang, Jin-Ho, Campos, Marcelo L., Zemelis-Durfee, Starla, Al-Haddad, Jameel M., Jones, A. Daniel, Telewski, Frank W., Brandizzi, Federica, Howe, Gregg A., and Raines, ed., Christine. Sun . "Molecular cloning of the tomato Hairless gene implicates actin dynamics in trichome-mediated defense and mechanical properties of stem tissue". United Kingdom. doi:10.1093/jxb/erw292.
@article{osti_1608739,
title = {Molecular cloning of the tomato Hairless gene implicates actin dynamics in trichome-mediated defense and mechanical properties of stem tissue},
author = {Kang, Jin-Ho and Campos, Marcelo L. and Zemelis-Durfee, Starla and Al-Haddad, Jameel M. and Jones, A. Daniel and Telewski, Frank W. and Brandizzi, Federica and Howe, Gregg A. and Raines, ed., Christine},
abstractNote = {Abstract Trichomes are epidermal structures that provide a first line of defense against arthropod herbivores. The recessive hairless (hl) mutation in tomato (Solanum lycopersicum L.) causes severe distortion of trichomes on all aerial tissues, impairs the accumulation of sesquiterpene and polyphenolic compounds in glandular trichomes, and compromises resistance to the specialist herbivore Manduca sexta. Here, we demonstrate that the tomato Hl gene encodes a subunit (SRA1) of the highly conserved WAVE regulatory complex that controls nucleation of actin filaments in a wide range of eukaryotic cells. The tomato SRA1 gene spans a 42-kb region containing both Solyc11g013280 and Solyc11g013290. The hl mutation corresponds to a complex 3-kb deletion that removes the last exon of the gene. Expression of a wild-type SRA1 cDNA in the hl mutant background restored normal trichome development, accumulation of glandular trichome-derived metabolites, and resistance to insect herbivory. These findings establish a role for SRA1 in the development of tomato trichomes and also implicate the actin-cytoskeleton network in cytosolic control of specialized metabolism for plant defense. We also show that the brittleness of hl mutant stems is associated with altered mechanical and cell morphological properties of stem tissue, and demonstrate that this defect is directly linked to the mutation in SRA1.},
doi = {10.1093/jxb/erw292},
journal = {Journal of Experimental Botany},
number = 18,
volume = 67,
place = {United Kingdom},
year = {2016},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1093/jxb/erw292

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Cited by: 9 works
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    Works referencing / citing this record:

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