Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (8): 1604-1616.doi: 10.3864/j.issn.0578-1752.2025.08.011

• HORTICULTURE • Previous Articles     Next Articles

Functional Analysis of MADS-box Transcription Factor Gene CaAGL61 in Heat Tolerance of Pepper

WANG MengYuan1(), WEI QianRui1, LI HaiYan1, YANG QiaoMin1, YU Jun2, HUANG Wei1(), LU MingHui1()   

  1. 1 College of Horticulture, Northwest A&F University, Yangling 712100, Shaanxi
    2 Xingping Agro-Tech Extension and Service Center, Xingping 713100, Shaanxi
  • Received:2024-09-24 Accepted:2024-11-14 Online:2025-04-16 Published:2025-04-21
  • Contact: HUANG Wei, LU MingHui

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Abstract:

【Objective】 MADS-box transcription factors are one of the largest transcription factor families in plants, and play important roles in plant growth, development, and stress responses. Previously, based on transcriptome data of pepper, a heat-responsive gene, Agamous-like MADS-box protein61 (AGL61), was identified as a MADS-box transcription factor. However, the function of CaAGL61 in pepper heat stress remains unknown. In this study, we explored the molecular function of CaAGL61 in heat tolerance of pepper plants, providing the regulatory insights of CaAGL61 as a potential locus for genetic improvement. 【Method】 The SMART online tool was used to predict the conserved domain of CaAGL61, and a phylogenetic tree of AGL61 in pepper and other plant species was constructed using MEGA7. The expression pattern of CaAGL61 was analyzed by quantitative real-time PCR. The subcellular localization of CaAGL61 was examined in tobacco, and its transcriptional regulatory role was investigated using a yeast two-hybrid system (Y2H). The effects of CaAGL61 on heat tolerance of pepper were accessed using transgenic plants generated by virus-induced gene silencing (VIGS) and transient overexpression techniques.【Result】CaAGL61 encodes a protein of 179 amino acids, containing a MADS domain and exhibiting high evolutionary conservation. CaAGL61’s expressional level was relatively high in the flower of pepper, followed by the stem and fruit, and lowest in the root. Further analysis reveals that the expression of CaAGL61 increased along with flower maturation process, peaking in the anther during pollination and fruit setting. High temperature treatment at 45 ℃ significantly upregulates the expression of CaAGL61. Subcellular localization showed that CaAGL61 is located in the nucleus, and yeast transcriptional activation assays indicates that CaAGL61 has transcriptional activation activity. Silencing of CaAGL61 significantly enhances heat tolerance of pepper. Comparing with control, CaAGL61-silenced plants exhibit reduced wilting in plant growth points, lower relative electrolyte leakage, reduced content of malondialdehyde, and accumulation of dead cells and reactive oxygen species (ROS), and increased content of chlorophyll under heat stress. However, transient overexpression of CaAGL61 reduces the heat tolerance of pepper, indicated by more severe heat-stress damage, higher relative electrolyte leakage, increased content of malondialdehyde, and accumulation of dead cells and ROS, and decreased content of chlorophyll compared to control. 【Conclusion】A heat-responsive MADS-box transcription factor gene, CaAGL61, was identified in pepper. This gene negatively regulates pepper heat tolerance by exacerbating oxidative stress.

Key words: pepper, heat tolerance, MADS-box transcription factor, CaAGL61, negative regulation

Table 1

Sequences of PCR primers"

用途 Purpose 名称 Name 序列 Sequence (5′-3′)
亚细胞定位及基因过表达
Subcellular localization and
gene overexpression		 pART27-GFP-CaAGL61-F GATGAACTATACAAAGAATTCATGCAAAATCTACTTGTTGAAG
pART27-GFP-CaAGL61-R CAGGACTCTAGATTAGGTACCCTAAGCAAACAAAGCTTGAAAA
基因沉默
Gene-silencing		 TRV2:CaAGL61-F GCTCTAGAGTTCTCGTGTTGCCTCTATTG
TRV2:CaAGL61-R CGGGATCCGATGGTTCCGTGCATCTACTA
转录激活活性分析
Activity analysis of transcriptional activation		 BD-CaAGL61-F ATGGCCATGGAGGCCGAATTCATGCAAAATCTACTTGTTGAAG
BD-CaAGL61-R CCGCTGCAGGTCGACGGATCCCTAAGCAAACAAAGCTTGAAAAG
基因表达分析
Analysis of gene expression		 qCaAGL61-F GGCCTTATACCTGCGGAGAC
qCaAGL61-R GTCGAAGACCATCTCGACCC
qCaUbi3-F TGTCCATCTGCTCTCTGTTG
qCaUbi3-R CACCCCAAGCACAATAAGAC
qCaHsfA2-F GTAGCATCAGTAGCCACAGC
qCaHsfA2-R CAAGCAACTCTTCCCAAATA
qCaHsfA3-F CGAAAGTATGATGAAAGAAGAGG
qCaHsfA3-R ATAGTTGCCAAGACCACCC
qCaHsp70.1-F CAGGTGTGCTAGTTCAGGTGT
qCaHsp70.1-R TGACCTGAGGCACTCCTCTT

Fig. 1

Characterization of pepper CaAGL61 sequence A: Prediction of conservative domain; B: Analysis of phylogenetic relationship. Bolded in the figure shows AGL61 of pepper"

Fig. 2

Expression pattern analysis of CaAGL61 A: Expression in different tissues and organs of pepper; B: Expression in different parts of flower; C: Expression at different stages of flowering; D: Expression at different time points of heat stress. Different lowercase letters indicate the significant differences at P<0.05 level"

Fig. 3

Subcellular localization of CaAGL61 A: Subcellular localization of CaAGL61; B: DAPI staining. pART27-GFP: The negative control with empty vector; pART27-GFP-CaAGL61: The expression vector of CaAGL61. DAPI: Nuclear dye"

Fig. 4

Analysis of transcriptional activity of CaAGL61 pGBKT7-P53: The positive control; pGBKT7-empty: The negative control with empty vector; pGBKT7-CaAGL61: The expression vector of CaAGL61 gene"

Fig. 5

Phenotypic and silencing efficiency of CaAGL61-silenced peppers A: Phenotype of pepper seedlings with CaAGL61 gene-silenced; B: The silencing efficiency of CaAGL61. TRV2:00: The negative control seedlings with empty vector; TRV2:CaPDS: The positive control seedlings; TRV2:CaAGL61: Pepper seedlings with CaAGL61 gene-silenced. *: The significant difference at P<0.05 level. The same as below"

Fig. 6

Effects of CaAGL61-silencing on the heat tolerance of pepper A: Phenotype of peppers; B and C: Relative expression level of heat shock protein gene CaHSP70.1 and heat shock transcription factor gene CaHsfA3; D and E: Phenotype and total chlorophyll content of leaf round blades; F: Content of malondialdehyde (MDA) in pepper leaves; G: Relative conductivity of pepper leaves; H and I: Accumulation of dead cells in pepper leaves (trypan blue staining); J and K: Accumulation of reactive oxygen species (DAB staining). **: The significant difference at P<0.01 levels. The same as below"

Fig. 7

Effects of CaAGL61 transient-overexpression on the heat tolerance of pepper A: Relative expression level of CaAGL61; B: Phenotype of pepper plants; C and D: Relative expression level of heat shock transcription factor gene CaHsfA2 and heat shock protein gene CaHSP70.1; E and F: Phenotype and total chlorophyll content of leaf round blades; G: MDA (malondialdehyde) content in pepper leaves; H: Relative conductivity of pepper leaves; I and J: Accumulation of dead cells in pepper leaves (trypan blue staining); K and L: Accumulation of reactive oxygen species (DAB staining). pART27: The negative control seedlings with empty vector; pART27-CaAGL61: Pepper seedlings with CaAGL61 transient overexpression"

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