Mitochondria-Targeted SmsHSP24.1 Overexpression Stimulates Early Seedling Vigor and Stress Tolerance by Multi-Pathway Transcriptome-Reprogramming

Among the diverse array of heat shock proteins across the three domains of life, mitochondria-targeted small heat shock proteins (sHSPs) are evolved in the plant lineage. However, they remained mysterious and understudied. In this study, we reported a systematic study of a novel mitochondria-targete...

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Autores principales: Muslima Khatun, Bhabesh Borphukan, Iftekhar Alam, Chaman Ara Keya, Varakumar Panditi, Haseena Khan, Saaimatul Huq, Malireddy K. Reddy, Md. Salimullah
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Publicado: Frontiers Media S.A. 2021
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spelling oai:doaj.org-article:0209d1218a1c4bf1bbf6f487497e70bc2021-11-30T12:12:09ZMitochondria-Targeted SmsHSP24.1 Overexpression Stimulates Early Seedling Vigor and Stress Tolerance by Multi-Pathway Transcriptome-Reprogramming1664-462X10.3389/fpls.2021.741898https://doaj.org/article/0209d1218a1c4bf1bbf6f487497e70bc2021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fpls.2021.741898/fullhttps://doaj.org/toc/1664-462XAmong the diverse array of heat shock proteins across the three domains of life, mitochondria-targeted small heat shock proteins (sHSPs) are evolved in the plant lineage. However, they remained mysterious and understudied. In this study, we reported a systematic study of a novel mitochondria-targeted nuclear sHSP from eggplant (Solanum melongena L.; SmsHSP24.1). Differential expression of SmsHSP24.1 indicated its positive role exerted during stress conditions. Escherichia coli-BL21 cell line overexpressing the SmsHSP24.1 showed excellent thermo-tolerance ability, tolerating up to 52°C. Spectrometry and electron microscopy revealed a multimeric structure of the protein which acted as a molecular chaperone at high temperatures. Overexpression of SmsHSP24.1 significantly enhanced resistance against heat, drought, and salt stresses and showed rapid germination in constitutively overexpressed eggplant lines. RNA-seq analysis reveals an apparent upregulation of a set of reactive oxygen species (ROS) scavenging enzymes of the glutathione (GHS) pathway and mitochondrial electron transport chain (ETC). Significant upregulation was also observed in auxin biosynthesis and cell-wall remodeling transcripts in overexpressed lines. qPCR, biochemical and physiological analysis further aligned with the finding of transcriptome analysis and suggested an essential role of SmsHSP24.1 under various stress responses and positive physiological influence on the growth of eggplants. Therefore, this gene has immense potential in engineering stress-resilient crop plants.Muslima KhatunBhabesh BorphukanIftekhar AlamChaman Ara KeyaVarakumar PanditiHaseena KhanSaaimatul HuqMalireddy K. ReddyMd. SalimullahFrontiers Media S.A.articleeggplantmitochondriachaperonabiotic stressheat tolerancesmall heat shock proteinPlant cultureSB1-1110ENFrontiers in Plant Science, Vol 12 (2021)
institution DOAJ
collection DOAJ
language EN
topic eggplant
mitochondria
chaperon
abiotic stress
heat tolerance
small heat shock protein
Plant culture
SB1-1110
spellingShingle eggplant
mitochondria
chaperon
abiotic stress
heat tolerance
small heat shock protein
Plant culture
SB1-1110
Muslima Khatun
Bhabesh Borphukan
Iftekhar Alam
Chaman Ara Keya
Varakumar Panditi
Haseena Khan
Saaimatul Huq
Malireddy K. Reddy
Md. Salimullah
Mitochondria-Targeted SmsHSP24.1 Overexpression Stimulates Early Seedling Vigor and Stress Tolerance by Multi-Pathway Transcriptome-Reprogramming
description Among the diverse array of heat shock proteins across the three domains of life, mitochondria-targeted small heat shock proteins (sHSPs) are evolved in the plant lineage. However, they remained mysterious and understudied. In this study, we reported a systematic study of a novel mitochondria-targeted nuclear sHSP from eggplant (Solanum melongena L.; SmsHSP24.1). Differential expression of SmsHSP24.1 indicated its positive role exerted during stress conditions. Escherichia coli-BL21 cell line overexpressing the SmsHSP24.1 showed excellent thermo-tolerance ability, tolerating up to 52°C. Spectrometry and electron microscopy revealed a multimeric structure of the protein which acted as a molecular chaperone at high temperatures. Overexpression of SmsHSP24.1 significantly enhanced resistance against heat, drought, and salt stresses and showed rapid germination in constitutively overexpressed eggplant lines. RNA-seq analysis reveals an apparent upregulation of a set of reactive oxygen species (ROS) scavenging enzymes of the glutathione (GHS) pathway and mitochondrial electron transport chain (ETC). Significant upregulation was also observed in auxin biosynthesis and cell-wall remodeling transcripts in overexpressed lines. qPCR, biochemical and physiological analysis further aligned with the finding of transcriptome analysis and suggested an essential role of SmsHSP24.1 under various stress responses and positive physiological influence on the growth of eggplants. Therefore, this gene has immense potential in engineering stress-resilient crop plants.
format article
author Muslima Khatun
Bhabesh Borphukan
Iftekhar Alam
Chaman Ara Keya
Varakumar Panditi
Haseena Khan
Saaimatul Huq
Malireddy K. Reddy
Md. Salimullah
author_facet Muslima Khatun
Bhabesh Borphukan
Iftekhar Alam
Chaman Ara Keya
Varakumar Panditi
Haseena Khan
Saaimatul Huq
Malireddy K. Reddy
Md. Salimullah
author_sort Muslima Khatun
title Mitochondria-Targeted SmsHSP24.1 Overexpression Stimulates Early Seedling Vigor and Stress Tolerance by Multi-Pathway Transcriptome-Reprogramming
title_short Mitochondria-Targeted SmsHSP24.1 Overexpression Stimulates Early Seedling Vigor and Stress Tolerance by Multi-Pathway Transcriptome-Reprogramming
title_full Mitochondria-Targeted SmsHSP24.1 Overexpression Stimulates Early Seedling Vigor and Stress Tolerance by Multi-Pathway Transcriptome-Reprogramming
title_fullStr Mitochondria-Targeted SmsHSP24.1 Overexpression Stimulates Early Seedling Vigor and Stress Tolerance by Multi-Pathway Transcriptome-Reprogramming
title_full_unstemmed Mitochondria-Targeted SmsHSP24.1 Overexpression Stimulates Early Seedling Vigor and Stress Tolerance by Multi-Pathway Transcriptome-Reprogramming
title_sort mitochondria-targeted smshsp24.1 overexpression stimulates early seedling vigor and stress tolerance by multi-pathway transcriptome-reprogramming
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/0209d1218a1c4bf1bbf6f487497e70bc
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