A Rapid Alkalinization Factor-like Peptide EaF82 Impairs Tapetum Degeneration during Pollen Development through Induced ATP Deficiency
In plants, the timely degeneration of tapetal cells is essential for providing nutrients and other substances to support pollen development. Rapid alkalinization factors (RALFs) are small, cysteine-rich peptides known to be involved in various aspects of plant development and growth, as well as defe...
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MDPI AG
2023-06-01
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| Series: | Cells |
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| Online Access: | https://www.mdpi.com/2073-4409/12/11/1542 |
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| author | Chiu-Yueh Hung Farooqahmed S. Kittur Keely N. Wharton Makendra L. Umstead D’Shawna B. Burwell Martinique Thomas Qi Qi Jianhui Zhang Carla E. Oldham Kent O. Burkey Jianjun Chen Jiahua Xie |
| author_facet | Chiu-Yueh Hung Farooqahmed S. Kittur Keely N. Wharton Makendra L. Umstead D’Shawna B. Burwell Martinique Thomas Qi Qi Jianhui Zhang Carla E. Oldham Kent O. Burkey Jianjun Chen Jiahua Xie |
| author_sort | Chiu-Yueh Hung |
| collection | DOAJ |
| description | In plants, the timely degeneration of tapetal cells is essential for providing nutrients and other substances to support pollen development. Rapid alkalinization factors (RALFs) are small, cysteine-rich peptides known to be involved in various aspects of plant development and growth, as well as defense against biotic and abiotic stresses. However, the functions of most of them remain unknown, while no RALF has been reported to involve tapetum degeneration. In this study, we demonstrated that a novel cysteine-rich peptide, EaF82, isolated from shy-flowering ‘Golden Pothos’ (<i>Epipremnum aureum</i>) plants, is a RALF-like peptide and displays alkalinizing activity. Its heterologous expression in Arabidopsis delayed tapetum degeneration and reduced pollen production and seed yields. RNAseq, RT-qPCR, and biochemical analyses showed that overexpression of <i>EaF82</i> downregulated a group of genes involved in pH changes, cell wall modifications, tapetum degeneration, and pollen maturation, as well as seven endogenous Arabidopsis <i>RALF</i> genes, and decreased proteasome activity and ATP levels. Yeast two-hybrid screening identified AKIN10, a subunit of energy-sensing SnRK1 kinase, as its interacting partner. Our study reveals a possible regulatory role for RALF peptide in tapetum degeneration and suggests that EaF82 action may be mediated through AKIN10 leading to the alteration of transcriptome and energy metabolism, thereby causing ATP deficiency and impairing pollen development. |
| first_indexed | 2024-03-11T03:10:00Z |
| format | Article |
| id | doaj.art-d94e4246950c4b19872fe917fd55868c |
| institution | Directory Open Access Journal |
| issn | 2073-4409 |
| language | English |
| last_indexed | 2024-03-11T03:10:00Z |
| publishDate | 2023-06-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Cells |
| spelling | doaj.art-d94e4246950c4b19872fe917fd55868c2023-11-18T07:41:28ZengMDPI AGCells2073-44092023-06-011211154210.3390/cells12111542A Rapid Alkalinization Factor-like Peptide EaF82 Impairs Tapetum Degeneration during Pollen Development through Induced ATP DeficiencyChiu-Yueh Hung0Farooqahmed S. Kittur1Keely N. Wharton2Makendra L. Umstead3D’Shawna B. Burwell4Martinique Thomas5Qi Qi6Jianhui Zhang7Carla E. Oldham8Kent O. Burkey9Jianjun Chen10Jiahua Xie11Department of Pharmaceutical Sciences, Biomanufacturing Research Institute & Technology Enterprise, North Carolina Central University, Durham, NC 27707, USADepartment of Pharmaceutical Sciences, Biomanufacturing Research Institute & Technology Enterprise, North Carolina Central University, Durham, NC 27707, USADepartment of Pharmaceutical Sciences, Biomanufacturing Research Institute & Technology Enterprise, North Carolina Central University, Durham, NC 27707, USADepartment of Pharmaceutical Sciences, Biomanufacturing Research Institute & Technology Enterprise, North Carolina Central University, Durham, NC 27707, USADepartment of Pharmaceutical Sciences, Biomanufacturing Research Institute & Technology Enterprise, North Carolina Central University, Durham, NC 27707, USADepartment of Pharmaceutical Sciences, Biomanufacturing Research Institute & Technology Enterprise, North Carolina Central University, Durham, NC 27707, USADepartment of Pharmaceutical Sciences, Biomanufacturing Research Institute & Technology Enterprise, North Carolina Central University, Durham, NC 27707, USADepartment of Pharmaceutical Sciences, Biomanufacturing Research Institute & Technology Enterprise, North Carolina Central University, Durham, NC 27707, USADepartment of Pharmaceutical Sciences, Biomanufacturing Research Institute & Technology Enterprise, North Carolina Central University, Durham, NC 27707, USAUSDA-ARS Plant Science Research Unit and Department of Crop and Soil Sciences, North Carolina State University, Raleigh, NC 27695, USAMid-Florida Research and Education Center, Environmental Horticulture Department, Institute of Food and Agricultural Sciences, University of Florida, Apopka, FL 32703, USADepartment of Pharmaceutical Sciences, Biomanufacturing Research Institute & Technology Enterprise, North Carolina Central University, Durham, NC 27707, USAIn plants, the timely degeneration of tapetal cells is essential for providing nutrients and other substances to support pollen development. Rapid alkalinization factors (RALFs) are small, cysteine-rich peptides known to be involved in various aspects of plant development and growth, as well as defense against biotic and abiotic stresses. However, the functions of most of them remain unknown, while no RALF has been reported to involve tapetum degeneration. In this study, we demonstrated that a novel cysteine-rich peptide, EaF82, isolated from shy-flowering ‘Golden Pothos’ (<i>Epipremnum aureum</i>) plants, is a RALF-like peptide and displays alkalinizing activity. Its heterologous expression in Arabidopsis delayed tapetum degeneration and reduced pollen production and seed yields. RNAseq, RT-qPCR, and biochemical analyses showed that overexpression of <i>EaF82</i> downregulated a group of genes involved in pH changes, cell wall modifications, tapetum degeneration, and pollen maturation, as well as seven endogenous Arabidopsis <i>RALF</i> genes, and decreased proteasome activity and ATP levels. Yeast two-hybrid screening identified AKIN10, a subunit of energy-sensing SnRK1 kinase, as its interacting partner. Our study reveals a possible regulatory role for RALF peptide in tapetum degeneration and suggests that EaF82 action may be mediated through AKIN10 leading to the alteration of transcriptome and energy metabolism, thereby causing ATP deficiency and impairing pollen development.https://www.mdpi.com/2073-4409/12/11/1542ATP deficiencycysteine-rich peptide<i>Epipremnum aureum</i>kinase AKIN10pollen productionrapid alkalinization factor |
| spellingShingle | Chiu-Yueh Hung Farooqahmed S. Kittur Keely N. Wharton Makendra L. Umstead D’Shawna B. Burwell Martinique Thomas Qi Qi Jianhui Zhang Carla E. Oldham Kent O. Burkey Jianjun Chen Jiahua Xie A Rapid Alkalinization Factor-like Peptide EaF82 Impairs Tapetum Degeneration during Pollen Development through Induced ATP Deficiency Cells ATP deficiency cysteine-rich peptide <i>Epipremnum aureum</i> kinase AKIN10 pollen production rapid alkalinization factor |
| title | A Rapid Alkalinization Factor-like Peptide EaF82 Impairs Tapetum Degeneration during Pollen Development through Induced ATP Deficiency |
| title_full | A Rapid Alkalinization Factor-like Peptide EaF82 Impairs Tapetum Degeneration during Pollen Development through Induced ATP Deficiency |
| title_fullStr | A Rapid Alkalinization Factor-like Peptide EaF82 Impairs Tapetum Degeneration during Pollen Development through Induced ATP Deficiency |
| title_full_unstemmed | A Rapid Alkalinization Factor-like Peptide EaF82 Impairs Tapetum Degeneration during Pollen Development through Induced ATP Deficiency |
| title_short | A Rapid Alkalinization Factor-like Peptide EaF82 Impairs Tapetum Degeneration during Pollen Development through Induced ATP Deficiency |
| title_sort | rapid alkalinization factor like peptide eaf82 impairs tapetum degeneration during pollen development through induced atp deficiency |
| topic | ATP deficiency cysteine-rich peptide <i>Epipremnum aureum</i> kinase AKIN10 pollen production rapid alkalinization factor |
| url | https://www.mdpi.com/2073-4409/12/11/1542 |
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