The LpHsfA2-molecular module confers thermotolerance via fine tuning of its transcription in perennial ryegrass (Lolium perenne L.)

doi:10.1111/jipb.13789

J Integr Plant Biol. ›› 2024, Vol. 66 ›› Issue (11): 2346-2361.DOI: 10.1111/jipb.13789 cstr: 32098.14.jipb.13789

• Abiotic Stress Responses • Previous Articles Next Articles

The LpHsfA2-molecular module confers thermotolerance via fine tuning of its transcription in perennial ryegrass (Lolium perenne L.)

Guangjing Ma^1,2, Zhihao Liu³, Shurui Song^1,2, Jing Gao^1,2, Shujie Liao⁴, Shilong Cao⁴, Yan Xie¹, Liwen Cao¹, Longxing Hu⁴, Haichun Jing^5,6* and Liang Chen^1,6*

1. CAS Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China
2. University of Chinese Academy of Sciences, Beijing 100049, China
3. Key Laboratory of Edible Wild Plants Conservation and Utilization, Hubei Normal University, Huangshi 435002, China
4. Department of Pratacultural Sciences, College of Agronomy, Hunan Agricultural University, Changsha 410128, China
5. Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
6. Academician Workstation of Agricultural High‐tech Industrial Area of the Yellow River Delta, National Center of Technology Innovation for Comprehensive Utilization of Saline‐Alkali Land, Dongying 257300, China
^*Correspondences: Haichun Jing (hcjing@ibcas.ac.cn); Liang Chen (chenliang888@wbgcas.cn, Dr. Chen is fully responsible for the distribution of all materials associated with this article)

Received:2024-03-11 Accepted:2024-09-25 Online:2024-10-18 Published:2024-11-01
Supported by:
This work was supported by the National Key R&D Program of China (2022YFF1003200), the National Natural Science Foundation of China (NSFC) (Grant Nos. 32001394, 32102431 and 32101430), the Science & Technology Specific Projects in Agricultural High‐tech Industrial Demonstration Area of the Yellow River Delta (Grant No. 2022SZX13), the Strategic Priority Research Program of Chinese Academy of Sciences (Grant No. XDA26050201), and the Major Science and Technology Innovation Project of Shandong Province (2022LZGC018).

Abstract

Abstract: Temperature sensitivity and tolerance play a key role in plant survival and production. Perennial ryegrass (Lolium perenne L.), widely cultivated in cool-season for forage supply and turfgrass, is extremely susceptible to high temperatures, therefore serving as an excellent grass for dissecting the genomic and genetic basis of high-temperature adaptation. In this study, expression analysis revealed that LpHsfA2, an important gene associated with high-temperature tolerance in perennial ryegrass, is rapidly and substantially induced under heat stress. Additionally, heat-tolerant varieties consistently display elevated expression levels of LpHsfA2 compared with heat-sensitive ones. Comparative haplotype analysis of the LpHsfA2 promoter indicated an uneven distribution of two haplotypes (HsfA2^Hap1and HsfA2^Hap2) across varieties with differing heat tolerance. Specifically, the HsfA2^Hap1 allele is predominantly present in heat-tolerant varieties, while the HsfA2^Hap2 allele exhibits the opposite pattern. Overexpression of LpHsfA2 confers enhanced thermotolerance, whereas silencing of LpHsfA2 compromises heat tolerance. Furthermore, LpHsfA2 orchestrates its protective effects by directly binding to the promoters of LpHSP18.2 and LpAPX1 to activate their expression, preventing the non-specific misfolding of intracellular protein and the accumulation of reactive oxygen species in cells. Additionally, LpHsfA4 and LpHsfA5 were shown to engage directly with the promoter of LpHsfA2, upregulating its expression as well as the expression of LpHSP18.2 and LpAPX1, thus contributing to enhanced heat tolerance. Markedly, LpHsfA2 possesses autoregulatory ability by directly binding to its own promoter to modulate the self-transcription. Based on these findings, we propose a model for modulating the thermotolerance of perennial ryegrass by precisely regulating the expression of LpHsfA2. Collectively, these findings provide a scientific basis for the development of thermotolerant perennial ryegrass cultivars.

Key words: haplotype, heat shock transcription factors, heat tolerance, perennial ryegrass

Guangjing Ma, Zhihao Liu, Shurui Song, Jing Gao, Shujie Liao, Shilong Cao, Yan Xie, Liwen Cao, Longxing Hu, Haichun Jing, Liang Chen. The LpHsfA2-molecular module confers thermotolerance via fine tuning of its transcription in perennial ryegrass (Lolium perenne L.)[J]. J Integr Plant Biol., 2024, 66(11): 2346-2361.

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The LpHsfA2-molecular module confers thermotolerance via fine tuning of its transcription in perennial ryegrass (Lolium perenne L.)

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