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Assortment of Flowering Time and Immunity Alleles in Natural Arabidopsis thaliana Populations Suggests Immunity and Vegetative Lifespan Strategies Coevolve.

ABSTRACT: The selective impact of pathogen epidemics on host defenses can be strong but remains transient. By contrast, life-history shifts can durably and continuously modify the balance between costs and benefits of immunity, which arbitrates the evolution of host defenses. Their impact on the evolutionary dynamics of host immunity, however, has seldom been documented. Optimal investment into immunity is expected to decrease with shortening lifespan, because a shorter life decreases the probability to encounter pathogens or enemies. Here, we document that in natural populations of Arabidopsis thaliana, the expression levels of immunity genes correlate positively with flowering time, which in annual species is a proxy for lifespan. Using a novel genetic strategy based on bulk-segregants, we partitioned flowering time-dependent from -independent immunity genes and could demonstrate that this positive covariation can be genetically separated. It is therefore not explained by the pleiotropic action of some major regulatory genes controlling both immunity and lifespan. Moreover, we find that immunity genes containing variants reported to impact fitness in natural field conditions are among the genes whose expression covaries most strongly with flowering time. Taken together, these analyses reveal that natural selection has likely assorted alleles promoting lower expression of immunity genes with alleles that decrease the duration of vegetative lifespan in A. thaliana and vice versa. This is the first study documenting a pattern of variation consistent with the impact that selection on flowering time is predicted to have on diversity in host immunity.

SUBMITTER: Glander S

PROVIDER: S-EPMC6133262 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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Assortment of Flowering Time and Immunity Alleles in Natural Arabidopsis thaliana Populations Suggests Immunity and Vegetative Lifespan Strategies Coevolve.

Glander Shirin S He Fei F Schmitz Gregor G Witten Anika A Telschow Arndt A de Meaux Juliette J

Genome biology and evolution 20180901 9

The selective impact of pathogen epidemics on host defenses can be strong but remains transient. By contrast, life-history shifts can durably and continuously modify the balance between costs and benefits of immunity, which arbitrates the evolution of host defenses. Their impact on the evolutionary dynamics of host immunity, however, has seldom been documented. Optimal investment into immunity is expected to decrease with shortening lifespan, because a shorter life decreases the probability to e ...[more]

PMID: 30215800

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Project description:Experimental studies of the flowering of Arabidopsis thaliana have shown that a large complex gene regulatory network (GRN) is responsible for its regulation. This process has been mathematically modelled with deterministic differential equations by considering the interactions between gene activators and inhibitors (Valentim et al. in PLoS ONE 10(2):e0116973, 2015; van Mourik et al. in BMC Syst Biol 4(1):1, 2010). However, due to complexity of the model, the properties of the network and the roles of the individual genes cannot be deducted from the numerical solution the published work offers. Here, we propose simplifications of the model, based on decoupling of the original GRN to motifs, described with three and two differential equations. A stable solution of the original model is sought by linearisation of the original model which contributes to further investigation of the role of the individual genes to the flowering. Furthermore, we study the role of noise by introducing and investigating two types of stochastic elements into the model. The deterministic and stochastic nonlinear dynamic models of Arabidopsis flowering time are considered by following the deterministic delayed model introduced in Valentim et al. (2015). Steady-state regimes and stability of the deterministic original model are investigated analytically and numerically. By decoupling some concentrations, the system was reduced to emphasise the role played by the transcription factor Suppressor of Overexpression of Constants1 ([Formula: see text]) and the important floral meristem identity genes, Leafy ([Formula: see text]) and Apetala1 ([Formula: see text]). Two-dimensional motifs, based on the dynamics of [Formula: see text] and [Formula: see text], are obtained from the reduced network and parameter ranges ensuring flowering are determined. Their stability analysis shows that [Formula: see text] and [Formula: see text] are regulating each other for flowering, matching experimental findings. New sufficient conditions of mean square stability in the stochastic model are obtained using a stochastic Lyapunov approach. Our numerical simulations demonstrate that the reduced models of Arabidopsis flowering time, describing specific motifs of the GRN, can capture the essential behaviour of the full system and also introduce the conditions of flowering initiation. Additionally, they show that stochastic effects can change the behaviour of the stability region through a stability switch. This study thus contributes to a better understanding of the role of [Formula: see text] and [Formula: see text] in Arabidopsis flowering.

Dataset Information

Assortment of Flowering Time and Immunity Alleles in Natural Arabidopsis thaliana Populations Suggests Immunity and Vegetative Lifespan Strategies Coevolve.

Publications

Assortment of Flowering Time and Immunity Alleles in Natural Arabidopsis thaliana Populations Suggests Immunity and Vegetative Lifespan Strategies Coevolve.

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