Genome-Wide Identification of the PAP Gene Family in Potatoes and Its Expression Response to Phosphorus-Solubilizing Bacteria, Freezing Stresses, and Phytohormonal Regulation

Purple acid phosphatases (PAPs) are multifunctional proteins implicated in various aspects of plant biology, including flowering, seed development, senescence, carbon metabolism, and the response to biotic and abiotic stresses. Although PAPs have been reported in potatoes, the gene features and expression under phosphorus-solubilizing bacteria and freezing stresses remain unclear. In the present study, we identified 29 StPAPs with molecular weights ranging from 27.96 to 85.40 kDa, which were classified into three distinct groups based on a phylogenetic analysis. Integrating gene chromosomal localization, gene duplication events, intergenic collinearity, and gene selection pressure analysis, we found that the expansion of the potato PAP gene family was primarily driven by genome-wide duplication events, with the majority of the PAP genes undergoing purifying selection. Promoter cis-acting element analysis and RNA-Seq data revealed that a total of 89 cis-acting elements were associated with plant hormones, and the seven StPAP genes for low phosphorous response were associated with responses to abscisic acid, gibberellin, and abiotic stresses. Tissue expression pattern analyses indicated that the expression of StPAP genes were regulated in response to varying phosphorus levels. A co-expression network analysis identified eight StPAP genes involved in symbiosis with phosphorus-solubilizing bacteria, and seven StPAP genes exhibited significantly higher expression in response to freezing stress and abiotic stresses (drought, heat, darkness, and N/K/Ca/Fe/Mg/Zn deficiencies). In conclusion, the StPAP may synergistically modulate phytohormone levels in response to stress by regulating plant phosphorus homeostasis; StPAP12 and abscisic acid are key phosphorus-regulated genes and phytohormones in response to freezing stress. This study represents the first report to demonstrating the responsiveness of StPAPs to phytohormones, revealing a potential new function for these genes in plant stress responses and nutrient management. These findings provide novel insights into the multifaceted roles of PAPs in plant adaptation and stress tolerance.

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Publication Details

Journal
Agronomy
Published
2024-11-20
DOI
https://doi.org/10.3390/agronomy14112735
Citations
2
Primary Topic
Plant nutrient uptake and metabolism
Type
article
Field-Weighted Citation Impact
1.20

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article

Genome-Wide Identification of the PAP Gene Family in Potatoes and Its Expression Response to Phosphorus-Solubilizing Bacteria, Freezing Stresses, and Phytohormonal Regulation

Hairong Luo, Kun Yang, Haicui Suo, C. Y. Li et al.
2 citations
Agronomy
Plant nutrient uptake and metabolism
1.20
article

Genome-Wide Identification of the PAP Gene Family in Potatoes and Its Expression Response to Phosphorus-Solubilizing Bacteria, Freezing Stresses, and Phytohormonal Regulation

Hairong Luo, Kun Yang, Haicui Suo, C. Y. Li, Yongshan Liao, Xiaobo Li, Kang An, Jianwei Shan, Jitao Liu, Li Wang
article en
2 citations

Abstract

Purple acid phosphatases (PAPs) are multifunctional proteins implicated in various aspects of plant biology, including flowering, seed development, senescence, carbon metabolism, and the response to biotic and abiotic stresses. Although PAPs have been reported in potatoes, the gene features and expression under phosphorus-solubilizing bacteria and freezing stresses remain unclear. In the present study, we identified 29 StPAPs with molecular weights ranging from 27.96 to 85.40 kDa, which were classified into three distinct groups based on a phylogenetic analysis. Integrating gene chromosomal localization, gene duplication events, intergenic collinearity, and gene selection pressure analysis, we found that the expansion of the potato PAP gene family was primarily driven by genome-wide duplication events, with the majority of the PAP genes undergoing purifying selection. Promoter cis-acting element analysis and RNA-Seq data revealed that a total of 89 cis-acting elements were associated with plant hormones, and the seven StPAP genes for low phosphorous response were associated with responses to abscisic acid, gibberellin, and abiotic stresses. Tissue expression pattern analyses indicated that the expression of StPAP genes were regulated in response to varying phosphorus levels. A co-expression network analysis identified eight StPAP genes involved in symbiosis with phosphorus-solubilizing bacteria, and seven StPAP genes exhibited significantly higher expression in response to freezing stress and abiotic stresses (drought, heat, darkness, and N/K/Ca/Fe/Mg/Zn deficiencies). In conclusion, the StPAP may synergistically modulate phytohormone levels in response to stress by regulating plant phosphorus homeostasis; StPAP12 and abscisic acid are key phosphorus-regulated genes and phytohormones in response to freezing stress. This study represents the first report to demonstrating the responsiveness of StPAPs to phytohormones, revealing a potential new function for these genes in plant stress responses and nutrient management. These findings provide novel insights into the multifaceted roles of PAPs in plant adaptation and stress tolerance.

AgronomyVol. 14(11)
Guangdong Academy of Agricultural Sciences (CN)
Natural Science Foundation of Guangdong Province, Basic and Applied Basic Research Foundation of Guangdong Province
Clean water and sanitation
Openalex Percentile: Top 16%
Plant nutrient uptake and metabolism
1.20
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