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Cultivar-biased regulation of HSFA7 and HSFB4a govern high-temperature tolerance in tomato

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Abstract

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Cultivar-biased regulation of HSFB4a and HSFA7 mediates heat stress tolerance/sensitivity in tomato. Reduced HSFB4a repressor levels and enhanced HSFA7 activator levels govern thermo-tolerance in tolerant cultivars.

Abstract

Heat shock factors (HSFs) are at the core of heat stress (HS) response in plants. However, the contribution of HSFs governing the inherent thermo-tolerance mechanism in tomato from sub-tropical hot climates is poorly understood. With the above aim, comparative expression profiles of the HSF family in a HS-tolerant (CLN1621L) and -sensitive cultivars (CA4 and Pusa Ruby) of tomato under HS revealed cultivar-biased regulation of an activator (HSFA7) and a repressor (HSFB4a) class HSF. HSFA7 exhibited strong upregulation while HSFB4a showed downregulation in tolerant tomato cultivar upon HS. Functional characterization of HSFA7 and HSFB4a in a tolerant–sensitive cultivar pair by virus-induced gene silencing (VIGS)-based silencing and transient overexpression established them as a positive and a negative regulator of HS tolerance, respectively. Promoter:GUS reporter assays and promoter sequence analyses suggest heat-mediated transcriptional control of both the HSF genes in the contrasting cultivars. Moreover, degradome data highlighted HSFB4a is a probable target of microRNA Sly-miR4200. Transient in-planta Sly-MIR4200-effector:HSFB4a-reporter assays showed miRNA-dependent target down-regulation. Chelation of miRNA by short-tandem-target-mimic of Sly-miR4200 increased target abundance, highlighting a link between Sly-miR4200 and HSFB4a. This miRNA has induced several folds upon HS in the tolerant cultivar where HSFB4a levels are reduced, thus exhibiting the inverse miR:target expression. Thus, we speculate that the alleviation of HSFB4a and increased HSFA7 levels govern thermo-tolerance in the tolerant cultivar by regulating downstream heat stress-responsive genes.

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Data availability

Derived data supporting the findings of this study are available from the corresponding author upon reasonable request.

Abbreviations

HS:

Heat Stress

HSF:

Heat Shock Factor

HSP:

Heat Shock Protein

HSR:

Heat Stress Response

ROS:

Reactive Oxygen Species

STTM:

Short-Tandem-Target-Mimic

TF:

Transcription factor

TRV VIGS:

Tobacco Rattle Virus-Induced Gene Silencing

VC:

Vector Control

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Acknowledgements

NIPGR and DST-SERB, India (Project No.: EMR/2016/006229) funded and supported this work. The authors acknowledge phytotron facility, CIF and field area provided by NIPGR. CLN1621L and CA4 seeds were obtained from AVRDC, Taiwan. Pusa Ruby seeds were obtained from Indian Agricultural Research Institute, Pusa, New Delhi, India. The authors are thankful to DBT-eLibrary Consortium (DeLCON) for providing access to e-resources. SR acknowledges Department of Biotechnology (DBT) Govt. of India and JRD acknowledges Council of Scientific and Industrial Research (CSIR) for the award of research fellowships.

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Correspondence to Saloni Mathur.

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The authors declare no conflict of interest.

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Communicated by Dorothea Bartels.

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Rao, S., Das, J.R., Balyan, S. et al. Cultivar-biased regulation of HSFA7 and HSFB4a govern high-temperature tolerance in tomato. Planta 255, 31 (2022). https://doi.org/10.1007/s00425-021-03813-y

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  • DOI: https://doi.org/10.1007/s00425-021-03813-y

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