New insights into plant natriuretic peptide evolution: From the lysogenic conversion in Xanthomonas to the lateral transfer to the whitefly Bemisia tabaci

Detalhes bibliográficos
Autor(a) principal: Patané, José S.L.
Data de Publicação: 2022
Outros Autores: Moreira, Leandro M., de Melo Teixeira, Marcus, Martins Jr, Joaquim, Setubal, João C., Varani, Alessandro M. [UNESP]
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1016/j.gene.2022.146326
http://hdl.handle.net/11449/231621
Resumo: Plant natriuretic peptide-like (PNP) are signaling molecules related to adaptive responses to stress. The Arabidopsis thaliana PNP (AtPNP-A) is capable of modulating catalase 2 (CAT2) and rubisco activase (RCA) activity in some circumstances. Interestingly, many plant-pathogens co-opted PNP-like molecules to their benefit. For instance, the citrus pathogen Xanthomonas citri carries a PNP-like (XacPNP) that can mimic and regulate plant homeostasis, and many phytopathogenic fungi carry effectors (e.g., Ave1 and AvrLm6) that are indeed PNP-like homologs. This work investigates the PNP-like evolution across the tree of life, revealing many parallel gains and duplications in plant and fungi kingdoms. All PNP-like proteins in the final dataset are structurally similar, containing the AtPNP-A active domains modulating CAT2 activity and RCA interaction. Comparative genomics evinced that XacPNP is a lysogenic conversion factor associated with a Myoviridae-like prophage identified in many Xanthomonas species. Surprisingly, a PNP-like homolog was identified in Bemisia tabaci, an important agricultural pest, being to date the second example of lateral gene transfer (LGT) from plant to the whitefly. Moreover, the Bemisia PNP-like homolog can also be considered a potential new effector of this phloem-feeding insect. Noteworthy, the whiteflies infest many plants carrying PNP-like copies and interact with some of their bacterial and fungal pathogens, strongly suggesting complex recipient/donor traits of PNP by LGT and bringing new insights into the evolution of host-pathogen arms race across the tree of life.
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spelling New insights into plant natriuretic peptide evolution: From the lysogenic conversion in Xanthomonas to the lateral transfer to the whitefly Bemisia tabaciEffectorsGenome evolutionLateral gene transferPlant-insect interactionsPlant-pathogen interactionsTransductionPlant natriuretic peptide-like (PNP) are signaling molecules related to adaptive responses to stress. The Arabidopsis thaliana PNP (AtPNP-A) is capable of modulating catalase 2 (CAT2) and rubisco activase (RCA) activity in some circumstances. Interestingly, many plant-pathogens co-opted PNP-like molecules to their benefit. For instance, the citrus pathogen Xanthomonas citri carries a PNP-like (XacPNP) that can mimic and regulate plant homeostasis, and many phytopathogenic fungi carry effectors (e.g., Ave1 and AvrLm6) that are indeed PNP-like homologs. This work investigates the PNP-like evolution across the tree of life, revealing many parallel gains and duplications in plant and fungi kingdoms. All PNP-like proteins in the final dataset are structurally similar, containing the AtPNP-A active domains modulating CAT2 activity and RCA interaction. Comparative genomics evinced that XacPNP is a lysogenic conversion factor associated with a Myoviridae-like prophage identified in many Xanthomonas species. Surprisingly, a PNP-like homolog was identified in Bemisia tabaci, an important agricultural pest, being to date the second example of lateral gene transfer (LGT) from plant to the whitefly. Moreover, the Bemisia PNP-like homolog can also be considered a potential new effector of this phloem-feeding insect. Noteworthy, the whiteflies infest many plants carrying PNP-like copies and interact with some of their bacterial and fungal pathogens, strongly suggesting complex recipient/donor traits of PNP by LGT and bringing new insights into the evolution of host-pathogen arms race across the tree of life.Departamento de Bioquímica Instituto de Química Universidade de São Paulo, SPDepartamento de Ciências Biológicas e Núcleo de Pesquisas em Ciências Biológicas Universidade Federal de Ouro Preto, MGFaculdade de Medicina Universidade de Brasília-DFUniversidade Estadual Paulista (UNESP) Faculdade de Ciências Agrárias e Veterinárias, SPUniversidade Estadual Paulista (UNESP) Faculdade de Ciências Agrárias e Veterinárias, SPUniversidade de São Paulo (USP)Universidade Federal de Ouro PretoUniversidade de Brasília (UnB)Universidade Estadual Paulista (UNESP)Patané, José S.L.Moreira, Leandro M.de Melo Teixeira, MarcusMartins Jr, JoaquimSetubal, João C.Varani, Alessandro M. [UNESP]2022-04-29T08:46:37Z2022-04-29T08:46:37Z2022-05-05info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1016/j.gene.2022.146326Gene, v. 821.1879-00380378-1119http://hdl.handle.net/11449/23162110.1016/j.gene.2022.1463262-s2.0-85124940882Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengGeneinfo:eu-repo/semantics/openAccess2022-04-29T08:46:37Zoai:repositorio.unesp.br:11449/231621Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T23:07:51.805960Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv New insights into plant natriuretic peptide evolution: From the lysogenic conversion in Xanthomonas to the lateral transfer to the whitefly Bemisia tabaci
title New insights into plant natriuretic peptide evolution: From the lysogenic conversion in Xanthomonas to the lateral transfer to the whitefly Bemisia tabaci
spellingShingle New insights into plant natriuretic peptide evolution: From the lysogenic conversion in Xanthomonas to the lateral transfer to the whitefly Bemisia tabaci
Patané, José S.L.
Effectors
Genome evolution
Lateral gene transfer
Plant-insect interactions
Plant-pathogen interactions
Transduction
title_short New insights into plant natriuretic peptide evolution: From the lysogenic conversion in Xanthomonas to the lateral transfer to the whitefly Bemisia tabaci
title_full New insights into plant natriuretic peptide evolution: From the lysogenic conversion in Xanthomonas to the lateral transfer to the whitefly Bemisia tabaci
title_fullStr New insights into plant natriuretic peptide evolution: From the lysogenic conversion in Xanthomonas to the lateral transfer to the whitefly Bemisia tabaci
title_full_unstemmed New insights into plant natriuretic peptide evolution: From the lysogenic conversion in Xanthomonas to the lateral transfer to the whitefly Bemisia tabaci
title_sort New insights into plant natriuretic peptide evolution: From the lysogenic conversion in Xanthomonas to the lateral transfer to the whitefly Bemisia tabaci
author Patané, José S.L.
author_facet Patané, José S.L.
Moreira, Leandro M.
de Melo Teixeira, Marcus
Martins Jr, Joaquim
Setubal, João C.
Varani, Alessandro M. [UNESP]
author_role author
author2 Moreira, Leandro M.
de Melo Teixeira, Marcus
Martins Jr, Joaquim
Setubal, João C.
Varani, Alessandro M. [UNESP]
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Universidade de São Paulo (USP)
Universidade Federal de Ouro Preto
Universidade de Brasília (UnB)
Universidade Estadual Paulista (UNESP)
dc.contributor.author.fl_str_mv Patané, José S.L.
Moreira, Leandro M.
de Melo Teixeira, Marcus
Martins Jr, Joaquim
Setubal, João C.
Varani, Alessandro M. [UNESP]
dc.subject.por.fl_str_mv Effectors
Genome evolution
Lateral gene transfer
Plant-insect interactions
Plant-pathogen interactions
Transduction
topic Effectors
Genome evolution
Lateral gene transfer
Plant-insect interactions
Plant-pathogen interactions
Transduction
description Plant natriuretic peptide-like (PNP) are signaling molecules related to adaptive responses to stress. The Arabidopsis thaliana PNP (AtPNP-A) is capable of modulating catalase 2 (CAT2) and rubisco activase (RCA) activity in some circumstances. Interestingly, many plant-pathogens co-opted PNP-like molecules to their benefit. For instance, the citrus pathogen Xanthomonas citri carries a PNP-like (XacPNP) that can mimic and regulate plant homeostasis, and many phytopathogenic fungi carry effectors (e.g., Ave1 and AvrLm6) that are indeed PNP-like homologs. This work investigates the PNP-like evolution across the tree of life, revealing many parallel gains and duplications in plant and fungi kingdoms. All PNP-like proteins in the final dataset are structurally similar, containing the AtPNP-A active domains modulating CAT2 activity and RCA interaction. Comparative genomics evinced that XacPNP is a lysogenic conversion factor associated with a Myoviridae-like prophage identified in many Xanthomonas species. Surprisingly, a PNP-like homolog was identified in Bemisia tabaci, an important agricultural pest, being to date the second example of lateral gene transfer (LGT) from plant to the whitefly. Moreover, the Bemisia PNP-like homolog can also be considered a potential new effector of this phloem-feeding insect. Noteworthy, the whiteflies infest many plants carrying PNP-like copies and interact with some of their bacterial and fungal pathogens, strongly suggesting complex recipient/donor traits of PNP by LGT and bringing new insights into the evolution of host-pathogen arms race across the tree of life.
publishDate 2022
dc.date.none.fl_str_mv 2022-04-29T08:46:37Z
2022-04-29T08:46:37Z
2022-05-05
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1016/j.gene.2022.146326
Gene, v. 821.
1879-0038
0378-1119
http://hdl.handle.net/11449/231621
10.1016/j.gene.2022.146326
2-s2.0-85124940882
url http://dx.doi.org/10.1016/j.gene.2022.146326
http://hdl.handle.net/11449/231621
identifier_str_mv Gene, v. 821.
1879-0038
0378-1119
10.1016/j.gene.2022.146326
2-s2.0-85124940882
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Gene
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
repository.mail.fl_str_mv
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