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Research article2021Peer reviewedOpen access

Natural variation in temperature-modulated immunity uncovers transcription factor bHLH059 as a thermoresponsive regulator in Arabidopsis thaliana

Bruessow, Friederike; Bautor, Jaqueline; Hoffmann, Gesa; Yildiz, Ipek; Zeier, Jurgen; Parker, Jane E.

Abstract

Author summaryTemperature has a profound effect on plant innate immune responses but little is known about the mechanisms underlying natural variation in transmission of temperature signals to defence pathways. Much of our understanding of temperature effects on plant immunity and tradeoffs between activated defences and growth has come from analysis of the common Arabidopsis thaliana genetic accession, Col-0. Here we examine A. thaliana genetic variation in response to temperature (within the non-stress range-22 C-o and 16 C-o) at the level of accumulation of the thermoresponsive biotic stress hormone salicylic acid (SA), bacterial pathogen resistance, and plant biomass. From analysis of 105 genetically diverse A. thaliana accessions we uncover plasticity in temperature-modulated SA homeostasis and in the relationship between SA levels and plant growth. We find that high SA amounts prior to infection provide a robust benefit of enhancing bacterial resistance. In some accessions this benefit comes without compromised plant growth, suggestive of altered defence-growth tradeoffs. Based on a temperature x SA association study we identify the transcription factor gene, bHLH059, and show that it has features of a temperature-sensitive immunity regulator that are unrelated to PIF4, a known thermosensitive coordinator of immunity and growth.Temperature impacts plant immunity and growth but how temperature intersects with endogenous pathways to shape natural variation remains unclear. Here we uncover variation between Arabidopsis thaliana natural accessions in response to two non-stress temperatures (22 degrees C and 16 degrees C) affecting accumulation of the thermoresponsive stress hormone salicylic acid (SA) and plant growth. Analysis of differentially responding A. thaliana accessions shows that pre-existing SA provides a benefit in limiting infection by Pseudomonas syringae pathovar tomato DC3000 bacteria at both temperatures. Several A. thaliana genotypes display a capacity to mitigate negative effects of high SA on growth, indicating within-species plasticity in SA-growth tradeoffs. An association study of temperature x SA variation, followed by physiological and immunity phenotyping of mutant and over-expression lines, identifies the transcription factor bHLH059 as a temperature-responsive SA immunity regulator. Here we reveal previously untapped diversity in plant responses to temperature and a way forward in understanding the genetic architecture of plant adaptation to changing environments.

Published in

PLOS GENETICS
2021, Volume: 17, number: 1, article number: e1009290
Publisher: PUBLIC LIBRARY SCIENCE

    Associated SLU-program

    SLU Plant Protection Network

    UKÄ Subject classification

    Genetics

    Publication identifier

    DOI: https://doi.org/10.1371/journal.pgen.1009290

    Permanent link to this page (URI)

    https://res.slu.se/id/publ/110987