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Title: Pith–specific lignification in Nicotiana attenuata as a defense against a stem–boring herbivore

Abstract

Plants have developed tissue-specific defense strategies in response to various herbivores with different feeding habits. Although defense responses to leaf-chewing insects have been well studied, little is known about stem-specific responses, particularly in the pith, to stem-boring herbivores. To understand the stem-specific defense, we first conducted a comparative transcriptomic analysis of the wild tobacco Nicotiana attenuata before and after attack by the leaf-chewing herbivore Manduca sexta and the stem borer Trichobaris mucorea. When the stem-boring herbivore attacked, lignin-associated genes were upregulated specifically in the inner parenchymal cells of the stem, the pith; lignin also accumulated highly in the attacked pith. Silencing the lignin biosynthetic gene cinnamyl alcohol dehydrogenase enhanced the performance of the stem-boring herbivore but had no effect on the growth of the leaf-chewing herbivore. Two-dimensional nuclear magnetic resonance results revealed that lignified pith contains feruloyltyramine as an unusual lignin component in the cell wall, as a response against stem-boring herbivore attack. Pith-specific lignification induced by the stem-boring herbivore was modulated by both jasmonate and ethylene signaling. Furthermore, these results suggest that lignin provides a stem-specific inducible barrier, protecting plants against stem-boring insects.

Authors:
 [1];  [2];  [3];  [4]; ORCiD logo [3];  [5];  [6];  [7];  [2]; ORCiD logo [5]; ORCiD logo [3]
  1. Max Planck Inst. for Chemical Ecology, Jena (Germany); Korea Advanced Inst. for Science and Technology, Daejeon (Korea); Chungbuk National Univ., Cheongju (Korea)
  2. Univ. of Wisconsin, Madison, WI (United States)
  3. Korea Advanced Inst. for Science and Technology, Daejeon (Korea)
  4. Max Planck Inst. for Chemical Ecology, Jena (Germany); Korea Advanced Inst. for Science and Technology, Daejeon (Korea)
  5. Max Planck Inst. for Chemical Ecology, Jena (Germany)
  6. Graduate School of International Agricultural Technology Seoul National University Pyoeng‐Chang 25354 Korea
  7. Seoul National Univ., Pyoeng‐Chang (Korea)
Publication Date:
Research Org.:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1827412
Grant/Contract Number:  
SC0018409
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 232; Journal Issue: 1; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Cinnamyl alcohol dehydrogenase (CAD); ethylene; feruloyltyramine; herbivore-induced lignification; jasmonate; pith; plant defense; Trichobaris mucorea

Citation Formats

Joo, Youngsung, Kim, Hoon, Kang, Moonyoung, Lee, Gisuk, Choung, Sungjun, Kaur, Harleen, Oh, Shinyoung, Choi, Jun Weon, Ralph, John, Baldwin, Ian T., and Kim, Sang‐Gyu. Pith–specific lignification in Nicotiana attenuata as a defense against a stem–boring herbivore. United States: N. p., 2021. Web. doi:10.1111/nph.17583.
Joo, Youngsung, Kim, Hoon, Kang, Moonyoung, Lee, Gisuk, Choung, Sungjun, Kaur, Harleen, Oh, Shinyoung, Choi, Jun Weon, Ralph, John, Baldwin, Ian T., & Kim, Sang‐Gyu. Pith–specific lignification in Nicotiana attenuata as a defense against a stem–boring herbivore. United States. https://doi.org/10.1111/nph.17583
Joo, Youngsung, Kim, Hoon, Kang, Moonyoung, Lee, Gisuk, Choung, Sungjun, Kaur, Harleen, Oh, Shinyoung, Choi, Jun Weon, Ralph, John, Baldwin, Ian T., and Kim, Sang‐Gyu. Fri . "Pith–specific lignification in Nicotiana attenuata as a defense against a stem–boring herbivore". United States. https://doi.org/10.1111/nph.17583. https://www.osti.gov/servlets/purl/1827412.
@article{osti_1827412,
title = {Pith–specific lignification in Nicotiana attenuata as a defense against a stem–boring herbivore},
author = {Joo, Youngsung and Kim, Hoon and Kang, Moonyoung and Lee, Gisuk and Choung, Sungjun and Kaur, Harleen and Oh, Shinyoung and Choi, Jun Weon and Ralph, John and Baldwin, Ian T. and Kim, Sang‐Gyu},
abstractNote = {Plants have developed tissue-specific defense strategies in response to various herbivores with different feeding habits. Although defense responses to leaf-chewing insects have been well studied, little is known about stem-specific responses, particularly in the pith, to stem-boring herbivores. To understand the stem-specific defense, we first conducted a comparative transcriptomic analysis of the wild tobacco Nicotiana attenuata before and after attack by the leaf-chewing herbivore Manduca sexta and the stem borer Trichobaris mucorea. When the stem-boring herbivore attacked, lignin-associated genes were upregulated specifically in the inner parenchymal cells of the stem, the pith; lignin also accumulated highly in the attacked pith. Silencing the lignin biosynthetic gene cinnamyl alcohol dehydrogenase enhanced the performance of the stem-boring herbivore but had no effect on the growth of the leaf-chewing herbivore. Two-dimensional nuclear magnetic resonance results revealed that lignified pith contains feruloyltyramine as an unusual lignin component in the cell wall, as a response against stem-boring herbivore attack. Pith-specific lignification induced by the stem-boring herbivore was modulated by both jasmonate and ethylene signaling. Furthermore, these results suggest that lignin provides a stem-specific inducible barrier, protecting plants against stem-boring insects.},
doi = {10.1111/nph.17583},
journal = {New Phytologist},
number = 1,
volume = 232,
place = {United States},
year = {Fri Jun 25 00:00:00 EDT 2021},
month = {Fri Jun 25 00:00:00 EDT 2021}
}

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