Conditional sanctioning in a legume– Rhizobium mutualism

Abstract

Legumes are high in protein and form a valuable part of human diets due to their interaction with symbiotic nitrogen-fixing bacteria known as rhizobia. Plants house rhizobia in specialized root nodules and provide the rhizobia with carbon in return for nitrogen. However, plants usually house multiple rhizobial strains that vary in their fixation ability, so the plant faces an investment dilemma. Plants are known to sanction strains that do not fix nitrogen, but nonfixers are rare in field settings, while intermediate fixers are common. Here, we modeled how plants should respond to an intermediate fixer that was otherwise isogenic and tested model predictions using pea plants. Intermediate fixers were only tolerated when a better strain was not available. In agreement with model predictions, nodules containing the intermediate-fixing strain were large and healthy when the only alternative was a nonfixer, but nodules of the intermediate-fixing strain were small and white when the plant was coinoculated with a more effective strain. The reduction in nodule size was preceded by a lower carbon supply to the nodule even before differences in nodule size could be observed. Sanctioned nodules had reduced rates of nitrogen fixation, and in later developmental stages, sanctioned nodules contained fewer viable bacteria than nonsanctioned nodules. This indicates that legumes can make conditional decisions, most likely by comparing a local nodule-dependent cue of nitrogen output with a global cue, giving them remarkable control over their symbiotic partners.

Competition, Nodule Occupancy, and Persistence of Inoculant Strains: Key Factors in the Rhizobium-Legume Symbioses

“…This dynamism over time and life phase of the host plant has been reported in the nodule microbiome of M. sativa , indicating that its members strongly interact through cooperation and competition ( Hansen et al, 2020 ). In fact, pea plants have been shown to tolerate intermediate fixers only when a better strain was not available ( Westhoek et al, 2021 ). Post-infection plant control over bacteroid metabolism is essential due to the high fitness cost of nodule formation and bacteroid maintenance.…”

“…The plant host must therefore monitor symbiotic performance and respond accordingly ( Ledermann et al, 2021 ). However, plants cannot select effective nitrogen-fixing rhizobia from a mixture of effective and ineffective strains in the soil in the early stages of the symbiotic interaction ( Westhoek et al, 2021 ). Instead, to avoid cheaters displacing effective symbionts once the infection has occurred, legumes limit cheating through host sanctions, which reduce the fitness of cheaters, and partner choice, where each partner can identify and reject forming relationships with cheaters ( West et al, 2002 ; Kiers et al, 2003 ; Kiers and Denison, 2008 ; Sachs et al, 2010 ; Oono et al, 2011 ; Daubech et al, 2017 ; Westhoek et al, 2021 ).…”

“…However, plants cannot select effective nitrogen-fixing rhizobia from a mixture of effective and ineffective strains in the soil in the early stages of the symbiotic interaction ( Westhoek et al, 2021 ). Instead, to avoid cheaters displacing effective symbionts once the infection has occurred, legumes limit cheating through host sanctions, which reduce the fitness of cheaters, and partner choice, where each partner can identify and reject forming relationships with cheaters ( West et al, 2002 ; Kiers et al, 2003 ; Kiers and Denison, 2008 ; Sachs et al, 2010 ; Oono et al, 2011 ; Daubech et al, 2017 ; Westhoek et al, 2021 ). Sanctioning of ineffective nodules occurs by reducing the number of viable cells present in nodules and reducing their reproductive success ( Kiers et al, 2003 ), by preferentially promoting nodule development in number and size with most BNF-efficient rhizobia due to the stimulation of plant cell multiplication and bacteroid differentiation ( Laguerre et al, 2012 ), or presumably by reducing resource allocation to a nodule and shutting it down ( Kiers et al, 2003 ; Westhoek et al, 2021 ).…”

“…Several rhizobia strains can inhabit nodules within the same host plant, even co-inhabiting the same nodule ( Mendoza-Suárez et al, 2020 ), and compete for host resources with non-fixing (“cheating”) strains ( Checcucci et al, 2017 ). However, it has been shown that plants can sanction nodules that are inefficient at fixing nitrogen ( Kiers et al, 2003 ; Regus et al, 2017 ; Westhoek et al, 2021 ). Moreover, legumes are able to control the number of nodules formed through an “autoregulation” process in which a shoot-derived signal limits infection ( Kinkema et al, 2006 ; Ferguson et al, 2010 ; Reid et al, 2011 ; Mortier et al, 2012 ).…”

Genetic Variation in Host-Specific Competitiveness of the Symbiont Rhizobium leguminosarum Symbiovar viciae

“…These mechanisms may result in the “sanction” of inefficient bacteria or may induce the senescence of symbiotic organs (for review, see Boivin and Lepetit, 2020 ). As symbiotic efficiency of bacteria varies according to its host, it is expected that sanction may depend not only on the microsymbiont but also probably of the plant partner ( Regus et al, 2017 ; Westhoek et al, 2021 ).…”