Cargando…

microRNA390 modulates Nicotiana attenuata's tolerance response to Manduca sexta herbivory

miR390 is a highly conserved miRNA in plant lineages known to function in growth and development processes, such as lateral root development, and in responses to salt and metal stress. In the ecological model species, Nicotiana attenuata, miR390's biological function remains unknown, which we e...

Descripción completa

Detalles Bibliográficos
Autores principales: Pradhan, Maitree, Rocha, Catarina, Halitschke, Rayko, Baldwin, Ian T., Pandey, Shree P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8482963/
https://www.ncbi.nlm.nih.gov/pubmed/34622121
http://dx.doi.org/10.1002/pld3.350
_version_ 1784577020039004160
author Pradhan, Maitree
Rocha, Catarina
Halitschke, Rayko
Baldwin, Ian T.
Pandey, Shree P.
author_facet Pradhan, Maitree
Rocha, Catarina
Halitschke, Rayko
Baldwin, Ian T.
Pandey, Shree P.
author_sort Pradhan, Maitree
collection PubMed
description miR390 is a highly conserved miRNA in plant lineages known to function in growth and development processes, such as lateral root development, and in responses to salt and metal stress. In the ecological model species, Nicotiana attenuata, miR390's biological function remains unknown, which we explore here with a gain‐of‐function analysis with plants over‐expressing (OE‐) N. attenuata miR390 (Na‐miR390) in glasshouse and natural environments. OEmiR390 plants showed normal developmental processes, including lateral root formation or reproductive output, in plants grown under standard conditions in the glasshouse. OEmiR390 plants did not have dramatically altered interactions with arbuscular mycorrhizal fungi (AMF), Fusarium pathogens, or herbivores. However, Na‐miR390 regulated the plant's tolerance of herbivory. Caterpillar feeding elicits the accumulation of a suite of phytohormones, including auxin and jasmonates, which further regulate host‐tolerance. The increase in Na‐miR390 abundance reduces the accumulation of auxin but does not influence levels of other phytohormones including jasmonates (JA, JA‐Ile), salicylic acid (SA), and abscisic acid (ABA). Na‐miR390 overexpression reduces reproductive output, quantified as capsule production, when plants are attacked by herbivores. Exogenous auxin treatments of herbivore‐attacked plants restored capsule production to wild‐type levels. During herbivory, Na‐miR390 transcript abundances are increased; its overexpression reduces the abundances of auxin biosynthesizing YUCCA and ARF (mainly ARF4) transcripts during herbivory. Furthermore, the accumulation of auxin‐regulated phenolamide secondary metabolites (caffeoylputrescine, dicaffeoylspermidine) is also reduced. In N. attenuata, miR390 functions in modulating tolerance responses of herbivore‐attacked plants.
format Online
Article
Text
id pubmed-8482963
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-84829632021-10-06 microRNA390 modulates Nicotiana attenuata's tolerance response to Manduca sexta herbivory Pradhan, Maitree Rocha, Catarina Halitschke, Rayko Baldwin, Ian T. Pandey, Shree P. Plant Direct Original Research miR390 is a highly conserved miRNA in plant lineages known to function in growth and development processes, such as lateral root development, and in responses to salt and metal stress. In the ecological model species, Nicotiana attenuata, miR390's biological function remains unknown, which we explore here with a gain‐of‐function analysis with plants over‐expressing (OE‐) N. attenuata miR390 (Na‐miR390) in glasshouse and natural environments. OEmiR390 plants showed normal developmental processes, including lateral root formation or reproductive output, in plants grown under standard conditions in the glasshouse. OEmiR390 plants did not have dramatically altered interactions with arbuscular mycorrhizal fungi (AMF), Fusarium pathogens, or herbivores. However, Na‐miR390 regulated the plant's tolerance of herbivory. Caterpillar feeding elicits the accumulation of a suite of phytohormones, including auxin and jasmonates, which further regulate host‐tolerance. The increase in Na‐miR390 abundance reduces the accumulation of auxin but does not influence levels of other phytohormones including jasmonates (JA, JA‐Ile), salicylic acid (SA), and abscisic acid (ABA). Na‐miR390 overexpression reduces reproductive output, quantified as capsule production, when plants are attacked by herbivores. Exogenous auxin treatments of herbivore‐attacked plants restored capsule production to wild‐type levels. During herbivory, Na‐miR390 transcript abundances are increased; its overexpression reduces the abundances of auxin biosynthesizing YUCCA and ARF (mainly ARF4) transcripts during herbivory. Furthermore, the accumulation of auxin‐regulated phenolamide secondary metabolites (caffeoylputrescine, dicaffeoylspermidine) is also reduced. In N. attenuata, miR390 functions in modulating tolerance responses of herbivore‐attacked plants. John Wiley and Sons Inc. 2021-09-30 /pmc/articles/PMC8482963/ /pubmed/34622121 http://dx.doi.org/10.1002/pld3.350 Text en © 2021 The Authors. Plant Direct published by American Society of Plant Biologists and the Society for Experimental Biology and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Original Research
Pradhan, Maitree
Rocha, Catarina
Halitschke, Rayko
Baldwin, Ian T.
Pandey, Shree P.
microRNA390 modulates Nicotiana attenuata's tolerance response to Manduca sexta herbivory
title microRNA390 modulates Nicotiana attenuata's tolerance response to Manduca sexta herbivory
title_full microRNA390 modulates Nicotiana attenuata's tolerance response to Manduca sexta herbivory
title_fullStr microRNA390 modulates Nicotiana attenuata's tolerance response to Manduca sexta herbivory
title_full_unstemmed microRNA390 modulates Nicotiana attenuata's tolerance response to Manduca sexta herbivory
title_short microRNA390 modulates Nicotiana attenuata's tolerance response to Manduca sexta herbivory
title_sort microrna390 modulates nicotiana attenuata's tolerance response to manduca sexta herbivory
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8482963/
https://www.ncbi.nlm.nih.gov/pubmed/34622121
http://dx.doi.org/10.1002/pld3.350
work_keys_str_mv AT pradhanmaitree microrna390modulatesnicotianaattenuatastoleranceresponsetomanducasextaherbivory
AT rochacatarina microrna390modulatesnicotianaattenuatastoleranceresponsetomanducasextaherbivory
AT halitschkerayko microrna390modulatesnicotianaattenuatastoleranceresponsetomanducasextaherbivory
AT baldwiniant microrna390modulatesnicotianaattenuatastoleranceresponsetomanducasextaherbivory
AT pandeyshreep microrna390modulatesnicotianaattenuatastoleranceresponsetomanducasextaherbivory