Facing constant challenges from various pathogens and pests, plants have evolved different strategies to defend themselves both locally and systemically. A global change in RNA metabolism is one of the necessary steps to mount a long-lasting immunity against present and future invasions.Arabidopsisserine/arginine-rich 45 (SR45) is an evolutionarily conserved RNA-binding protein that regulates multiple steps of RNA metabolism. Our prior study suggested that SR45 acts as a negative regulator of plant immunity. To better understand the molecular mechanism for SR45’s defense role, we examined the metabolic profile in both Col-0 andsr45-1. The results showed a significant accumulation of pipecolic acid (Pip), salicylic acid (SA), and other potential defense compounds insr45-1, indicating an increased systemic immunity. Thesr45–1mutant exhibited an elevated resistance to a wide range of biotrophic pathogen species and insensitivity to Pip, SA, and pathogen pretreatment. Between the two alternatively spliced isoforms, SR45.1 and SR45.2, SR45.1 seemed to be the culprit for the observed immune suppression. Upon examination of the transcriptome profile between Col-0 andsr45-1under either mock orPseudomonas syringae PmaDG3 challenge, we identified 1,125 genes as SR45-suppressed andPmaDG3-induced. Genes that function in SA biosynthesis and systemic acquired resistance were overrepresented, including those coding for WRKY, receptor-like kinases (RLKs), receptor-like proteins (RLPs), protein kinases, and TIR-NBS-LRR proteins. In addition, we identified significant alternative splicing activity in a list of genes due to eithersr45–1alone or bothsr45–1andPmaDG3 challenge. Among them, we characterized the effect of alternative splicing in two candidates,CBRLK1andSRF1. Interestingly, alternative splicing in both exhibited a switch between RLPs and RLKs in the predicted protein products. Overexpressing theirsr45–1dominant isoform in Col-0 led to a partial increase in immunity, suggesting the involvement of both alternative splicing events in SR45-conferred immune suppression. In summary, we hypothesize that SR45 regulates a subset of immune genes at either transcriptional or co-transcriptional pre-mRNA splicing levels to confer its function in systemic immune suppression.
more »
« less
Pathogen‐driven coevolution across the CBP60 plant immune regulator subfamilies confers resilience on the regulator module
Summary Components of the plant immune signaling network need mechanisms that confer resilience against fast‐evolving pathogen effectors that target them. Among eight Arabidopsis CaM‐Binding Protein (CBP) 60 family members, AtCBP60g and AtSARD1 are partially functionally redundant, major positive immune regulators, and AtCBP60a is a negative immune regulator. We investigated possible resilience‐conferring evolutionary mechanisms among the CBP60a, CBP60g and SARD1 immune regulatory subfamilies.Phylogenetic analysis was used to investigate the times of CBP60 subfamily neofunctionalization. Then, using the pairwise distance rank based on the newly developed analytical platform Protein Evolution Analysis in a Euclidean Space (PEAES), hypotheses of specific coevolutionary mechanisms that could confer resilience on the regulator module were tested.The immune regulator subfamilies diversified around the time of angiosperm divergence and have been evolving very quickly. We detected significant coevolutionary interactions across the immune regulator subfamilies in all of 12 diverse core eudicot species lineages tested. The coevolutionary interactions were consistent with the hypothesized coevolution mechanisms.Despite their unusually fast evolution, members across the CBP60 immune regulator subfamilies have influenced the evolution of each other long after their diversification in a way that could confer resilience on the immune regulator module against fast‐evolving pathogen effectors.
more »
« less
- Award ID(s):
- 1645460
- PAR ID:
- 10374344
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 233
- Issue:
- 1
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- p. 479-495
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract In insects and other invertebrates, prior pathogen exposures can improve immune responses and survival to subsequent infections through immune priming. Alternatively, stress and metabolic costs of multiple infections can impair host immunity and survival. The effects of high‐temperature extremes on host–pathogen interactions are not well understood despite the increasing occurrence of heat waves caused by climate change.The response of insects to heat waves and pathogens depends on recent evolutionary history with selective pressures. Domestication of insect pests has occurred in lab colonies of model species, reducing selective pressures for immune and heat stress responses. Lab strains are often used in immunological or heat stress experiments to represent wild field strains, but the efficacy of this approach is seldom evaluated.Using the tobacco hornworm (Manduca sexta), we tested the impact of a heat wave during initial pathogen exposure on survival of a secondary infection withBacillus thuringiensisbacteria. We used a domesticated lab population and a naturally occurring field population ofM. sextato evaluate the impacts of recent domestication on immune and thermal responses.A heat wave during initial infection significantly increased survival of the secondaryB. thuringiensisinfection in the field, but not the lab population ofM. sexta.In the field population, survival of the repeated infection was temperature dependent: exposure to an initial infection event reduced survival of the secondary infection at the control temperature regime, consistent with a stress effect. However, a heat wave during the initial infection event increased survival of the secondary infection, consistent with immune priming effects.The results of this study demonstrate that (a) insect response to thermal stress and pathogens can depend on recent domestication and (b) responses of hosts to repeat pathogen exposures can be temperature‐dependent, suggesting that cross‐talk between the heat stress and immune memory pathways may have important consequences for host–pathogen outcomes under heat wave events. Read the freePlain Language Summaryfor this article on the Journal blog.more » « less
-
Summary Arbuscular mycorrhizal fungi (AMF) are critical to native plant community ecology and influence plant invasions. Research has focused on nutritional benefits of AMF, although evidence shows that they may also confer pathogen resistance. However, most such work has focused on agriculturally relevant plant species. Therefore, whether AMF confer pathogen resistance tonative(wild) plant species, and impact of novel plant–microbial relationships on this benefit, remains understudied.We conducted a series of experiments measuring mycorrhizal‐induced resistance (MIR) to pathogens in native prairie plant species. We tested for pathogenicity across 69 field‐isolated fungi and oomycetes across five plant species. We then conducted experiments assessing growth response to native and non‐native AMF and pathogens in three plant species from native populations and milkweed (Asclepias syriaca) from native and postagricultural populations.We found evidence of MIR in milkweed. Moreover, we identified differential effects of AMF depending on plant species, with milkweed from native populations showing benefits from AMF. Finally, growth response was mediated by local adaptation, with matching AMF–pathogen origin strengthening responses.This work illustrates the importance of locally sourced AMF and plants to native plant ecology and suggests that pathogen resistance may be an important dimension of AMF benefit.more » « less
-
Abstract Biologists aim to explain patterns of growth, reproduction and ageing that characterize life histories, yet we are just beginning to understand the proximate mechanisms that generate this diversity. Existing research in this area has focused on telomeres but has generally overlooked the telomere's most direct mediator, the shelterin protein complex. Shelterin proteins physically interact with the telomere to shape its shortening and repair. They also regulate metabolism and immune function, suggesting a potential role in life history variation in the wild. However, research on shelterin proteins is uncommon outside of biomolecular work.Intraspecific analyses can play an important role in resolving these unknowns because they reveal subtle variation in life history within and among populations. Here, we assessed ecogeographic variation in shelterin protein abundance across eight populations of tree swallow (Tachycineta bicolor) with previously documented variation in environmental and life history traits. Using the blood gene expression of four shelterin proteins in 12‐day‐old nestlings, we tested the hypothesis that shelterin protein gene expression varies latitudinally and in relation to both telomere length and life history.Shelterin protein gene expression differed among populations and tracked non‐linear variation in latitude: nestlings from mid‐latitudes expressed nearly double the shelterin mRNA on average than those at more northern and southern sites. However, telomere length was not significantly related to latitude.We next assessed whether telomere length and shelterin protein gene expression correlate with 12‐day‐old body mass and wing length, two proxies of nestling growth linked to future fecundity and survival. We found that body mass and wing length correlated more strongly (and significantly) with shelterin protein gene expression than with telomere length.These results highlight telomere regulatory shelterin proteins as potential mediators of life history variation among populations. Together with existing research linking shelterin proteins and life history variation within populations, these ecogeographic patterns underscore the need for continued integration of ecology, evolution and telomere biology, which together will advance understanding of the drivers of life history variation in nature.more » « less
-
Abstract Plant nucleotide-binding, leucine-rich-repeat (NLR) immune receptors recognize pathogen effectors and activate immunity. The NLR RPS2 recognizes AvrRpt2, aPseudomonaseffector that promotes virulence by proteolytically cleaving a membrane-tethered host protein, RIN4. RIN4 cleavage by AvrRpt2 generates fragments that activate RPS2. A model for RPS2 activation by RIN4 destruction is consistent with the ectopic activity of RPS2 in plants lacking RIN4 but does not explain the link between AvrRpt2’s virulence activity and RPS2 activation. We found that non-membrane-tethered RIN4 derivatives are potent cytosolic activators of RPS2. Activation of RPS2 by these RIN4 derivatives, like AvrRpt2-induced activation, and unlike ectopic activation in the absence of RIN4, requires the defense signaling protein NDR1. Cleavage products of RIN4 produced by AvrRpt2 play contrasting roles in the activation of RPS2, with the membrane-tethered C-terminal fragment suppressing RPS2 and the non-membrane-tethered internal fragment, dependent on compatibility with the C-terminal fragment, overcoming its suppression of RPS2. HighlightsNon-membrane tethered derivatives of RIN4 activate RPS2-induced cell deathActivation of RPS2 by non-membrane-tethered derivatives of RIN4 requires NDR1AvrRpt2-induced cleavage fragments of RIN4 play contrasting roles in RPS2 activationmore » « less
An official website of the United States government
