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Comprehensive analysis of polygalacturonase gene family highlights candidate genes related to pollen development and male fertility in wheat (Triticum aestivum L.)

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Abstract

Main conclusion

Four polygalacturonase gene family members were highlighted that contribute to elucidate the roles of polygalacturonase during the fertility conversion process in male-sterile wheat.

Abstract

Polygalacturonase (PG) belongs to a large family of hydrolases with important functions in cell separation during plant growth and development via the degradation of pectin. Specific expressed PGs in anthers may be significant for male sterility research and hybrid wheat breeding, but they have not been characterized in wheat (Triticum aestivum L.). In this study, we systematically studied the PG gene family using the latest published wheat reference genomic information. In total, 113 wheat PG genes were identified, which could be classified into six categories A–F according to their structure characteristics and phylogenetic comparisons with Arabidopsis and rice. Polyploidy and segmental duplications in wheat were proved to be mainly responsible for the expansion of the wheat PG gene family. RNA-seq showed that TaPGs have specific temporal and spatial expression characteristics, in which 12 TaPGs with spike-specific expression patterns were detected by qRT-PCR in different fertility anthers of KTM3315A, a thermo-sensitive cytoplasmic male-sterile wheat. Four of them specific upregulated (TaPG09, TaPG95, and TaPG93) or downregulated (TaPG87) at trinucleate stage of fertile anthers, and further aligning with the homologous in Arabidopsis revealed that they may undertake functions such as anther dehiscence, separation of pollen, pollen development, and pollen tube elongation, thereby inducing male fertility conversion in KTM3315A. These findings facilitate function investigations of the wheat PG gene family and provide new insights into the fertility conversion mechanism in male-sterile wheat.

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Abbreviations

ADPG1(2):

Arabidopsis Dehiscence zone polygalacturonase 1(2)

PG:

Polygalacturonase

TaPG :

Triticum aestivum Polygalacturonase gene

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Acknowledgements

This work was supported by the National Natural Science Foundation of China [Grant number 31771874]; the Program in Science and Technology of Yangling State Demonstration Zone of Agricultural High-Tech Industries [Grant number 2018NY-19].

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  1. College of Agronomy, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Jiali Ye, Xuetong Yang, Zhiquan Yang, Fuqiang Niu, Yanru Chen, Lingli Zhang & Xiyue Song

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Supplementary file1 (RAR 384 kb)

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Supplementary file2 Fig. S1 The flow chart of identification of wheat PG gene family members. Bold fonts represent files used in the identification process, the red fonts represent the softwares (version) used in the identification process, and the e-values represent the threshold used in the corresponding step. Fig. S2 Chromosome locations of 113 TaPGs. Fig. S3 Rectangular layout of the PG gene family members in 13 plant species in the phylogenetic tree. Fig. S4 Numbers of PGs in each PG gene family class in wheat, Arabidopsis, and rice. The three bars in each category represent wheat, Arabidopsis, and rice from the top to the bottom. Fig. S5 Ten motif sequences in wheat PGs. Fig. S6 GO annotations obtained for TaPGs. The red, yellow, and green bars represent the cellular component, molecular function, and biological process annotations for the TaPGs, respectively. The numbers at the end of the bars represent the number of wheat PG genes enriched for the corresponding annotation. Fig. S7 Distribution of cis-elements for TaPGs. The cis-elements are explained by the different colored symbols at the bottom. Fig. S8 RT-PCR verification results. The annotation on the left represents the gene name, and the annotation on the bottom represents different tissues. AS represents anthers from sterile KTM3315A plants, AF represents anthers from fertile KTM3315A plants; 1, 2, and 3 represent the three anther development periods comprising the uninucleate, binucleate, and trinucleate stages, respectively; AFs and AFl represent the stems and leaves from fertile plants in the trinucleate stage, respectively; and AFg represents the grains from fertile plants three days after pollination. Actin as internal control. (RAR 1747 kb)

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Ye, J., Yang, X., Yang, Z. et al. Comprehensive analysis of polygalacturonase gene family highlights candidate genes related to pollen development and male fertility in wheat (Triticum aestivum L.). Planta 252, 31 (2020). https://doi.org/10.1007/s00425-020-03435-w

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