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Development and evolution of age-dependent defenses in ant-acacias.

ABSTRACT: Age-dependent changes in plant defense against herbivores are widespread, but why these changes exist remains a mystery. We explored this question by examining a suite of traits required for the interaction between swollen thorn acacias (genus Vachellia) and ants of the genus Pseudomyrmex In this system, plants provide ants with refuge and food in the form of swollen stipular spines, protein-lipid-rich "Beltian" bodies, and sugar-secreting extrafloral nectaries-the "swollen thorn syndrome." We show that this syndrome develops at a predictable time in shoot development and is tightly associated with the temporal decline in the microRNAs miR156 and miR157 and a corresponding increase in their targets-the SPL transcription factors. Growth under reduced light intensity delays both the decline in miR156/157 and the development of the swollen thorn syndrome, supporting the conclusion that these traits are controlled by the miR156-SPL pathway. Production of extrafloral nectaries by Vachellia sp. that do not house ants is also correlated with a decline in miR156/157, suggesting that this syndrome evolved by co-opting a preexisting age-dependent program. Along with genetic evidence from other model systems, these findings support the hypothesis that the age-dependent development of the swollen thorn syndrome is a consequence of genetic regulation rather than a passive developmental pattern arising from developmental constraints on when these traits can develop.

SUBMITTER: Leichty AR

PROVIDER: S-EPMC6681755 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Development and evolution of age-dependent defenses in ant-acacias.

Leichty Aaron R AR Poethig R Scott RS

Proceedings of the National Academy of Sciences of the United States of America 20190715 31

Age-dependent changes in plant defense against herbivores are widespread, but why these changes exist remains a mystery. We explored this question by examining a suite of traits required for the interaction between swollen thorn acacias (genus <i>Vachellia</i>) and ants of the genus <i>Pseudomyrmex</i> In this system, plants provide ants with refuge and food in the form of swollen stipular spines, protein-lipid-rich "Beltian" bodies, and sugar-secreting extrafloral nectaries-the "swollen thorn s ...[more]

PMID: 31308222

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Project description:In the course of an infection, Salmonella enterica occupies diverse anatomical sites with various concentrations of oxygen (O2) and nitric oxide (NO). These diatomic gases compete for binding to catalytic metal groups of quinol oxidases. Enterobacteriaceae express two evolutionarily distinct classes of quinol oxidases that differ in affinity for O2 and NO as well as stoichiometry of H+ translocated across the cytoplasmic membrane. The investigations presented here show that the dual function of bacterial cytochrome bd in bioenergetics and antinitrosative defense enhances Salmonella virulence. The high affinity of cytochrome bd for O2 optimizes respiratory rates in hypoxic cultures, and thus, this quinol oxidase maximizes bacterial growth under O2-limiting conditions. Our investigations also indicate that cytochrome bd, rather than cytochrome bo, is an intrinsic component of the adaptive antinitrosative toolbox of Salmonella Accordingly, induction of cytochrome bd helps Salmonella grow and respire in the presence of inhibitory NO. The combined antinitrosative defenses of cytochrome bd and the flavohemoglobin Hmp account for a great part of the adaptations that help Salmonella recover from the antimicrobial activity of NO. Moreover, the antinitrosative defenses of cytochrome bd and flavohemoglobin Hmp synergize to promote Salmonella growth in systemic tissues. Collectively, our investigations indicate that cytochrome bd is a critical means by which Salmonella resists the nitrosative stress that is engendered in the innate response of mammalian hosts while it concomitantly allows for proper O2 utilization in tissue hypoxia. It is becoming quite apparent that metabolism is critically important to the virulence potential of pathogenic microorganisms. Bacterial cells use a variety of terminal electron acceptors to power electron transport chains and metabolic processes. Of all the electron acceptors available to bacteria, utilization of O2 yields the most energy while diversifying the type of substrates that a pathogen can use. Recent investigations have demonstrated important roles for bd-type quinol oxidases with high affinity for O2 in bacterial pathogenesis. The investigations presented here have revealed that cytochrome bd potentiates virulence of a clinically relevant bacterial pathogen by fueling bioenergetics of prokaryotic cells while protecting the respiratory chain against NO toxicity. The adaptive antinitrosative defenses afforded by cytochrome bd synergize with other NO-detoxifying systems to preserve cellular bioenergetics, thereby promoting bacterial virulence in tissue hypoxia.

Dataset Information

Development and evolution of age-dependent defenses in ant-acacias.

Publications

Development and evolution of age-dependent defenses in ant-acacias.

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