Cargando…
LHT1/MAC7 contributes to proper alternative splicing under long-term heat stress and mediates variation in the heat tolerance of Arabidopsis
Natural genetic variation has facilitated the identification of genes underlying complex traits such as stress tolerances. We here evaluated the long-term (L-) heat tolerance (37°C for 5 days) of 174 Arabidopsis thaliana accessions and short-term (S-) heat tolerance (42°C, 50 min) of 88 accessions a...
Autores principales: | , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2023
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10644991/ https://www.ncbi.nlm.nih.gov/pubmed/38024403 http://dx.doi.org/10.1093/pnasnexus/pgad348 |
_version_ | 1785147304846557184 |
---|---|
author | Isono, Kazuho Nakamura, Kotaro Hanada, Kousuke Shirai, Kazumasa Ueki, Mao Tanaka, Keisuke Tsuchimatsu, Takashi Iuchi, Satoshi Kobayashi, Masatomo Yotsui, Izumi Sakata, Yoichi Taji, Teruaki |
author_facet | Isono, Kazuho Nakamura, Kotaro Hanada, Kousuke Shirai, Kazumasa Ueki, Mao Tanaka, Keisuke Tsuchimatsu, Takashi Iuchi, Satoshi Kobayashi, Masatomo Yotsui, Izumi Sakata, Yoichi Taji, Teruaki |
author_sort | Isono, Kazuho |
collection | PubMed |
description | Natural genetic variation has facilitated the identification of genes underlying complex traits such as stress tolerances. We here evaluated the long-term (L-) heat tolerance (37°C for 5 days) of 174 Arabidopsis thaliana accessions and short-term (S-) heat tolerance (42°C, 50 min) of 88 accessions and found extensive variation, respectively. Interestingly, L-heat–tolerant accessions are not necessarily S-heat tolerant, suggesting that the tolerance mechanisms are different. To elucidate the mechanisms underlying the variation, we performed a chromosomal mapping using the F(2) progeny of a cross between Ms-0 (a hypersensitive accession) and Col-0 (a tolerant accession) and found a single locus responsible for the difference in L-heat tolerance between them, which we named Long-term Heat Tolerance 1 (LHT1). LHT1 is identical to MAC7, which encodes a putative RNA helicase involved in mRNA splicing as a component of the MOS4 complex. We found one amino acid deletion in LHT1 of Ms-0 that causes a loss of function. Arabidopsis mutants of other core components of the MOS4 complex—mos4-2, cdc5-1, mac3a mac3b, and prl1 prl2—also showed hypersensitivity to L-heat stress, suggesting that the MOS4 complex plays an important role in L-heat stress responses. L-heat stress induced mRNA processing–related genes and compromised alternative splicing. Loss of LHT1 function caused genome-wide detrimental splicing events, which are thought to produce nonfunctional mRNAs that include retained introns under L-heat stress. These findings suggest that maintaining proper alternative splicing under L-heat stress is important in the heat tolerance of A. thaliana. |
format | Online Article Text |
id | pubmed-10644991 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-106449912023-11-14 LHT1/MAC7 contributes to proper alternative splicing under long-term heat stress and mediates variation in the heat tolerance of Arabidopsis Isono, Kazuho Nakamura, Kotaro Hanada, Kousuke Shirai, Kazumasa Ueki, Mao Tanaka, Keisuke Tsuchimatsu, Takashi Iuchi, Satoshi Kobayashi, Masatomo Yotsui, Izumi Sakata, Yoichi Taji, Teruaki PNAS Nexus Biological, Health, and Medical Sciences Natural genetic variation has facilitated the identification of genes underlying complex traits such as stress tolerances. We here evaluated the long-term (L-) heat tolerance (37°C for 5 days) of 174 Arabidopsis thaliana accessions and short-term (S-) heat tolerance (42°C, 50 min) of 88 accessions and found extensive variation, respectively. Interestingly, L-heat–tolerant accessions are not necessarily S-heat tolerant, suggesting that the tolerance mechanisms are different. To elucidate the mechanisms underlying the variation, we performed a chromosomal mapping using the F(2) progeny of a cross between Ms-0 (a hypersensitive accession) and Col-0 (a tolerant accession) and found a single locus responsible for the difference in L-heat tolerance between them, which we named Long-term Heat Tolerance 1 (LHT1). LHT1 is identical to MAC7, which encodes a putative RNA helicase involved in mRNA splicing as a component of the MOS4 complex. We found one amino acid deletion in LHT1 of Ms-0 that causes a loss of function. Arabidopsis mutants of other core components of the MOS4 complex—mos4-2, cdc5-1, mac3a mac3b, and prl1 prl2—also showed hypersensitivity to L-heat stress, suggesting that the MOS4 complex plays an important role in L-heat stress responses. L-heat stress induced mRNA processing–related genes and compromised alternative splicing. Loss of LHT1 function caused genome-wide detrimental splicing events, which are thought to produce nonfunctional mRNAs that include retained introns under L-heat stress. These findings suggest that maintaining proper alternative splicing under L-heat stress is important in the heat tolerance of A. thaliana. Oxford University Press 2023-11-14 /pmc/articles/PMC10644991/ /pubmed/38024403 http://dx.doi.org/10.1093/pnasnexus/pgad348 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of National Academy of Sciences. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
spellingShingle | Biological, Health, and Medical Sciences Isono, Kazuho Nakamura, Kotaro Hanada, Kousuke Shirai, Kazumasa Ueki, Mao Tanaka, Keisuke Tsuchimatsu, Takashi Iuchi, Satoshi Kobayashi, Masatomo Yotsui, Izumi Sakata, Yoichi Taji, Teruaki LHT1/MAC7 contributes to proper alternative splicing under long-term heat stress and mediates variation in the heat tolerance of Arabidopsis |
title |
LHT1/MAC7 contributes to proper alternative splicing under long-term heat stress and mediates variation in the heat tolerance of Arabidopsis |
title_full |
LHT1/MAC7 contributes to proper alternative splicing under long-term heat stress and mediates variation in the heat tolerance of Arabidopsis |
title_fullStr |
LHT1/MAC7 contributes to proper alternative splicing under long-term heat stress and mediates variation in the heat tolerance of Arabidopsis |
title_full_unstemmed |
LHT1/MAC7 contributes to proper alternative splicing under long-term heat stress and mediates variation in the heat tolerance of Arabidopsis |
title_short |
LHT1/MAC7 contributes to proper alternative splicing under long-term heat stress and mediates variation in the heat tolerance of Arabidopsis |
title_sort | lht1/mac7 contributes to proper alternative splicing under long-term heat stress and mediates variation in the heat tolerance of arabidopsis |
topic | Biological, Health, and Medical Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10644991/ https://www.ncbi.nlm.nih.gov/pubmed/38024403 http://dx.doi.org/10.1093/pnasnexus/pgad348 |
work_keys_str_mv | AT isonokazuho lht1mac7contributestoproperalternativesplicingunderlongtermheatstressandmediatesvariationintheheattoleranceofarabidopsis AT nakamurakotaro lht1mac7contributestoproperalternativesplicingunderlongtermheatstressandmediatesvariationintheheattoleranceofarabidopsis AT hanadakousuke lht1mac7contributestoproperalternativesplicingunderlongtermheatstressandmediatesvariationintheheattoleranceofarabidopsis AT shiraikazumasa lht1mac7contributestoproperalternativesplicingunderlongtermheatstressandmediatesvariationintheheattoleranceofarabidopsis AT uekimao lht1mac7contributestoproperalternativesplicingunderlongtermheatstressandmediatesvariationintheheattoleranceofarabidopsis AT tanakakeisuke lht1mac7contributestoproperalternativesplicingunderlongtermheatstressandmediatesvariationintheheattoleranceofarabidopsis AT tsuchimatsutakashi lht1mac7contributestoproperalternativesplicingunderlongtermheatstressandmediatesvariationintheheattoleranceofarabidopsis AT iuchisatoshi lht1mac7contributestoproperalternativesplicingunderlongtermheatstressandmediatesvariationintheheattoleranceofarabidopsis AT kobayashimasatomo lht1mac7contributestoproperalternativesplicingunderlongtermheatstressandmediatesvariationintheheattoleranceofarabidopsis AT yotsuiizumi lht1mac7contributestoproperalternativesplicingunderlongtermheatstressandmediatesvariationintheheattoleranceofarabidopsis AT sakatayoichi lht1mac7contributestoproperalternativesplicingunderlongtermheatstressandmediatesvariationintheheattoleranceofarabidopsis AT tajiteruaki lht1mac7contributestoproperalternativesplicingunderlongtermheatstressandmediatesvariationintheheattoleranceofarabidopsis |