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

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.17583· OSTI ID:1827412
 [1];  [2];  [3];  [4];  [3];  [5];  [6];  [7];  [2];  [5];  [3]
  1. Max Planck Inst. for Chemical Ecology, Jena (Germany); Korea Advanced Inst. for Science and Technology, Daejeon (Korea); Chungbuk National Univ., Cheongju (Korea); Max Planck Institute for Chemical Ecology Department of Molecular Ecology
  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)
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.
Research Organization:
Great Lakes Bioenergy Research Center, Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
SC0018409
OSTI ID:
1827412
Journal Information:
New Phytologist, Journal Name: New Phytologist Journal Issue: 1 Vol. 232; ISSN 0028-646X
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (65)

The role of lignin as a defence against the spruce bark beetle Dendroctonus micans: effect on larvae and adults journal December 1990
Agrobacterium-mediated transformation of Nicotiana attenuata, a model ecological expression system journal November 2002
Does lignin modification affect feeding preference or growth performance of insect herbivores in transgenic silver birch (Betula pendula Roth)? journal June 2005
A robust genome-editing method for wild plant species Nicotiana attenuata journal August 2020
Solution-state 2D NMR of Ball-milled Plant Cell Wall Gels in DMSO-d 6 journal March 2008
Ether-linked ferulic acid amides in natural and wound periderms of potato tuber journal December 1996
Wound-Induced Tyramine Hydroxycinnamoyl Transferase in Potato (Solanum tuberosum) Tuber discs journal November 1993
Designer lignins: harnessing the plasticity of lignification journal February 2016
Structural features and regulation of lignin deposited upon biotic and abiotic stresses journal April 2019
Compensated adiabatic inversion pulses: Broadband INEPT and HSQC journal August 2007
Redundancy and specificity in jasmonate signalling journal October 2016
Signatures of cinnamyl alcohol dehydrogenase deficiency in poplar lignins journal February 2004
Herbivore-associated elicitors: FAC signaling and metabolism journal June 2011
Role of phytohormones in insect-specific plant reactions journal May 2012
Lignin Monomers from beyond the Canonical Monolignol Biosynthetic Pathway: Another Brick in the Wall journal March 2020
JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling journal July 2007
DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins journal October 2015
Field and pulping performances of transgenic trees with altered lignification journal June 2002
Whole plant cell wall characterization using solution-state 2D NMR journal August 2012
Rice phenolamindes reduce the survival of female adults of the white-backed planthopper Sogatella furcifera journal April 2020
NMR analysis of lignins in CAD-deficient plants. Part 1. Incorporation of hydroxycinnamaldehydes and hydroxybenzaldehydes into lignins journal December 2002
Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6/pyridine-d5 journal January 2010
Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana: Alternative wound signalling pathways in Arabidopsis journal October 1999
Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent manner and identify jasmonate mutants in natural populations journal May 2012
Wild tobacco genomes reveal the evolution of nicotine biosynthesis journal May 2017
Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco journal August 2017
NMR characterization of altered lignins extracted from tobacco plants down-regulated for lignification enzymes cinnamylalcohol dehydrogenase and cinnamoyl-CoA reductase journal October 1998
Adaptive Patterns in Alkaloid Physiology journal May 1974
ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks journal February 2009
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal November 2009
STAR: ultrafast universal RNA-seq aligner journal October 2012
Genetic Modification of Lignin in Hybrid Poplar (Populus alba × Populus tremula) Does Not Substantially Alter Plant Defense or Arthropod Communities journal May 2017
On–Off Switches for Secondary Cell Wall Biosynthesis journal March 2012
Friends or Foes: New Insights in Jasmonate and Ethylene Co-Actions journal November 2014
R2R3-NaMYB8 Regulates the Accumulation of Phenylpropanoid-Polyamine Conjugates, Which Are Essential for Local and Systemic Defense against Insect Herbivores in Nicotiana attenuata journal January 2010
Jasmonic Acid and Ethylene Modulate Local Responses to Wounding and Simulated Herbivory in Nicotiana attenuata Leaves     journal April 2010
Pithy Protection: Nicotiana attenuata ’s Jasmonic Acid-Mediated Defenses Are Required to Resist Stem-Boring Weevil Larvae     journal February 2011
NaJAZh Regulates a Subset of Defense Responses against Herbivores and Spontaneous Leaf Necrosis in Nicotiana attenuata Plants journal April 2012
Environmental Stresses of Field Growth Allow Cinnamyl Alcohol Dehydrogenase-Deficient Nicotiana attenuata Plants to Compensate for their Structural Deficiencies journal May 2012
Induced Jasmonate Signaling Leads to Contrasting Effects on Root Damage and Herbivore Performance journal January 2015
Association of Caffeoyl Coenzyme A 3-O-Methyltransferase Expression with Lignifying Tissues in Several Dicot Plants journal December 1997
Molecular Interactions between the Specialist Herbivore Manduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata . I. Large-Scale Changes in the Accumulation of Growth- and Defense-Related Plant mRNAs journal February 2001
ETHYLENE RESPONSE FACTOR1 Integrates Signals from Ethylene and Jasmonate Pathways in Plant Defense journal December 2002
Arabidopsis Basic Helix-Loop-Helix Transcription Factors MYC2, MYC3, and MYC4 Regulate Glucosinolate Biosynthesis, Insect Performance, and Feeding Behavior journal August 2013
Interaction between MYC2 and ETHYLENE INSENSITIVE3 Modulates Antagonism between Jasmonate and Ethylene Signaling in Arabidopsis journal January 2014
The Jasmonate-Activated Transcription Factor MdMYC2 Regulates ETHYLENE RESPONSE FACTOR and Ethylene Biosynthetic Genes to Promote Ethylene Biosynthesis during Apple Fruit Ripening journal May 2017
Below-ground herbivory and root toughness: a potential model system using lignin-modified tobacco journal March 2010
The Arabidopsis cinnamoyl CoA reductase irx4 mutant has a delayed but coherent (normal) program of lignification journal December 2006
Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata: Ethylene biosynthesis during herbivory journal June 2007
Identification of the structure and origin of a thioacidolysis marker compound for ferulic acid incorporation into angiosperm lignins (and an indicator for cinnamoyl CoA reductase deficiency): Marker for ferulic acid incorporation into lignins journal October 2007
Shifting Nicotiana attenuata 's diurnal rhythm does not alter its resistance to the specialist herbivore Manduca sexta: N. attenuata 's resistance to M. sexta is diurnally robust journal February 2016
A simple, flexible and high-throughput cloning system for plant genome editing via CRISPR-Cas system: Single CRISPR-Cas binary vector for plant genome editing journal April 2016
Trichobaris weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval performance journal June 2016
Metabolomics reveals herbivore-induced metabolites of resistance and susceptibility in maize leaves and roots: Plant-insect metabolomics journal September 2012
Insect herbivory elicits genome-wide alternative splicing responses in Nicotiana attenuata journal October 2015
WRKY71 accelerates flowering via the direct activation of FLOWERING LOCUS T and LEAFY in Arabidopsis thaliana journal December 2015
What happens in the pith stays in the pith: tissue-localized defense responses facilitate chemical niche differentiation between two spatially separated herbivores journal September 2017
In planta gene targeting can be enhanced by the use of CRISPR/Cas12a journal September 2019
Molecular Interactions Between Plants and Insect Herbivores journal April 2019
High-throughput quantification of more than 100 primary- and secondary-metabolites, and phytohormones by a single solid-phase extraction based sample preparation with analysis by UHPLC–HESI–MS/MS journal May 2016
Strigolactone signaling regulates specialized metabolism in tobacco stems and interactions with stem-feeding herbivores journal August 2020
Impact of the Stem Borer, Dectes texanus , on Yield of the Cultivated Sunflower, Helianthus annuus . journal April 2007
Lignin Extraction and Quantification, a Tool to Monitor Defense Reaction at the Plant Cell Wall Level journal January 2015
Über die Ursache der Farbreaktionen des Holzes. journal January 1948
Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature journal October 2012