Unraveling a Tangled Skein: Evolutionary Analysis of the Bacterial Gibberellin Biosynthetic Operon

ABSTRACT Gibberellin (GA) phytohormones are ubiquitous regulators of growth and developmental processes in vascular plants. The convergent evolution of GA production by plant-associated bacteria, including both symbiotic nitrogen-fixing rhizobia and phytopathogens, suggests that manipulation of GA s...

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Autores principales:	Ryan S. Nett, Huy Nguyen, Raimund Nagel, Ariana Marcassa, Trevor C. Charles, Iddo Friedberg, Reuben J. Peters
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	gibberellin operon evolution plant-microbe interactions Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0bc73bd15da84de3a680e8275e164b59
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spelling	oai:doaj.org-article:0bc73bd15da84de3a680e8275e164b592021-11-15T15:30:15ZUnraveling a Tangled Skein: Evolutionary Analysis of the Bacterial Gibberellin Biosynthetic Operon10.1128/mSphere.00292-202379-5042https://doaj.org/article/0bc73bd15da84de3a680e8275e164b592020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00292-20https://doaj.org/toc/2379-5042ABSTRACT Gibberellin (GA) phytohormones are ubiquitous regulators of growth and developmental processes in vascular plants. The convergent evolution of GA production by plant-associated bacteria, including both symbiotic nitrogen-fixing rhizobia and phytopathogens, suggests that manipulation of GA signaling is a powerful mechanism for microbes to gain an advantage in these interactions. Although orthologous operons encode GA biosynthetic enzymes in both rhizobia and phytopathogens, notable genetic heterogeneity and scattered operon distribution in these lineages, including loss of the gene for the final biosynthetic step in most rhizobia, suggest varied functions for GA in these distinct plant-microbe interactions. Therefore, deciphering GA operon evolutionary history should provide crucial evidence toward understanding the distinct biological roles for bacterial GA production. To further establish the genetic composition of the GA operon, two operon-associated genes that exhibit limited distribution among rhizobia were biochemically characterized, verifying their roles in GA biosynthesis. This enabled employment of a maximum parsimony ancestral gene block reconstruction algorithm to characterize loss, gain, and horizontal gene transfer (HGT) of GA operon genes within alphaproteobacterial rhizobia, which exhibit the most heterogeneity among the bacteria containing this biosynthetic gene cluster. Collectively, this evolutionary analysis reveals a complex history for HGT of the entire GA operon, as well as the individual genes therein, and ultimately provides a basis for linking genetic content to bacterial GA functions in diverse plant-microbe interactions, including insight into the subtleties of the coevolving molecular interactions between rhizobia and their leguminous host plants. IMPORTANCE While production of phytohormones by plant-associated microbes has long been appreciated, identification of the gibberellin (GA) biosynthetic operon in plant-associated bacteria has revealed surprising genetic heterogeneity. Notably, this heterogeneity seems to be associated with the lifestyle of the microbe; while the GA operon in phytopathogenic bacteria does not seem to vary to any significant degree, thus enabling production of bioactive GA, symbiotic rhizobia exhibit a number of GA operon gene loss and gain events. This suggests that a unique set of selective pressures are exerted on this biosynthetic gene cluster in rhizobia. Through analysis of the evolutionary history of the GA operon in alphaproteobacterial rhizobia, which display substantial diversity in their GA operon structure and gene content, we provide insight into the effect of lifestyle and host interactions on the production of this phytohormone by plant-associated bacteria.Ryan S. NettHuy NguyenRaimund NagelAriana MarcassaTrevor C. CharlesIddo FriedbergReuben J. PetersAmerican Society for Microbiologyarticlegibberellinoperon evolutionplant-microbe interactionsMicrobiologyQR1-502ENmSphere, Vol 5, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	gibberellin operon evolution plant-microbe interactions Microbiology QR1-502
spellingShingle	gibberellin operon evolution plant-microbe interactions Microbiology QR1-502 Ryan S. Nett Huy Nguyen Raimund Nagel Ariana Marcassa Trevor C. Charles Iddo Friedberg Reuben J. Peters Unraveling a Tangled Skein: Evolutionary Analysis of the Bacterial Gibberellin Biosynthetic Operon
description	ABSTRACT Gibberellin (GA) phytohormones are ubiquitous regulators of growth and developmental processes in vascular plants. The convergent evolution of GA production by plant-associated bacteria, including both symbiotic nitrogen-fixing rhizobia and phytopathogens, suggests that manipulation of GA signaling is a powerful mechanism for microbes to gain an advantage in these interactions. Although orthologous operons encode GA biosynthetic enzymes in both rhizobia and phytopathogens, notable genetic heterogeneity and scattered operon distribution in these lineages, including loss of the gene for the final biosynthetic step in most rhizobia, suggest varied functions for GA in these distinct plant-microbe interactions. Therefore, deciphering GA operon evolutionary history should provide crucial evidence toward understanding the distinct biological roles for bacterial GA production. To further establish the genetic composition of the GA operon, two operon-associated genes that exhibit limited distribution among rhizobia were biochemically characterized, verifying their roles in GA biosynthesis. This enabled employment of a maximum parsimony ancestral gene block reconstruction algorithm to characterize loss, gain, and horizontal gene transfer (HGT) of GA operon genes within alphaproteobacterial rhizobia, which exhibit the most heterogeneity among the bacteria containing this biosynthetic gene cluster. Collectively, this evolutionary analysis reveals a complex history for HGT of the entire GA operon, as well as the individual genes therein, and ultimately provides a basis for linking genetic content to bacterial GA functions in diverse plant-microbe interactions, including insight into the subtleties of the coevolving molecular interactions between rhizobia and their leguminous host plants. IMPORTANCE While production of phytohormones by plant-associated microbes has long been appreciated, identification of the gibberellin (GA) biosynthetic operon in plant-associated bacteria has revealed surprising genetic heterogeneity. Notably, this heterogeneity seems to be associated with the lifestyle of the microbe; while the GA operon in phytopathogenic bacteria does not seem to vary to any significant degree, thus enabling production of bioactive GA, symbiotic rhizobia exhibit a number of GA operon gene loss and gain events. This suggests that a unique set of selective pressures are exerted on this biosynthetic gene cluster in rhizobia. Through analysis of the evolutionary history of the GA operon in alphaproteobacterial rhizobia, which display substantial diversity in their GA operon structure and gene content, we provide insight into the effect of lifestyle and host interactions on the production of this phytohormone by plant-associated bacteria.
format	article
author	Ryan S. Nett Huy Nguyen Raimund Nagel Ariana Marcassa Trevor C. Charles Iddo Friedberg Reuben J. Peters
author_facet	Ryan S. Nett Huy Nguyen Raimund Nagel Ariana Marcassa Trevor C. Charles Iddo Friedberg Reuben J. Peters
author_sort	Ryan S. Nett
title	Unraveling a Tangled Skein: Evolutionary Analysis of the Bacterial Gibberellin Biosynthetic Operon
title_short	Unraveling a Tangled Skein: Evolutionary Analysis of the Bacterial Gibberellin Biosynthetic Operon
title_full	Unraveling a Tangled Skein: Evolutionary Analysis of the Bacterial Gibberellin Biosynthetic Operon
title_fullStr	Unraveling a Tangled Skein: Evolutionary Analysis of the Bacterial Gibberellin Biosynthetic Operon
title_full_unstemmed	Unraveling a Tangled Skein: Evolutionary Analysis of the Bacterial Gibberellin Biosynthetic Operon
title_sort	unraveling a tangled skein: evolutionary analysis of the bacterial gibberellin biosynthetic operon
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/0bc73bd15da84de3a680e8275e164b59
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Unraveling a Tangled Skein: Evolutionary Analysis of the Bacterial Gibberellin Biosynthetic Operon

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