Microscopic and Transcriptomic Analyses of Dalbergoid Legume Peanut Reveal a Divergent Evolution Leading to Nod-Factor-Dependent Epidermal Crack-Entry and Terminal Bacteroid Differentiation
Root nodule symbiosis (RNS) is the pillar behind sustainable agriculture and plays a pivotal role in the environmental nitrogen cycle. Most of the genetic, molecular, and cell-biological knowledge on RNS comes from model legumes that exhibit a root-hair mode of bacterial infection, in contrast to th...
| Main Authors: | , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
The American Phytopathological Society
2022-02-01
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| Series: | Molecular Plant-Microbe Interactions |
| Subjects: | |
| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/MPMI-05-21-0122-R |
| _version_ | 1818647175274430464 |
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| author | Bikash Raul Oindrila Bhattacharjee Amit Ghosh Priya Upadhyay Kunal Tembhare Ajeet Singh Tarannum Shaheen Asim Kumar Ghosh Ivone Torres-Jerez Nick Krom Josh Clevenger Michael Udvardi Brian E. Scheffler Peggy Ozias-Akins Ravi Datta Sharma Kaustav Bandyopadhyay Vineet Gaur Shailesh Kumar Senjuti Sinharoy |
| author_facet | Bikash Raul Oindrila Bhattacharjee Amit Ghosh Priya Upadhyay Kunal Tembhare Ajeet Singh Tarannum Shaheen Asim Kumar Ghosh Ivone Torres-Jerez Nick Krom Josh Clevenger Michael Udvardi Brian E. Scheffler Peggy Ozias-Akins Ravi Datta Sharma Kaustav Bandyopadhyay Vineet Gaur Shailesh Kumar Senjuti Sinharoy |
| author_sort | Bikash Raul |
| collection | DOAJ |
| description | Root nodule symbiosis (RNS) is the pillar behind sustainable agriculture and plays a pivotal role in the environmental nitrogen cycle. Most of the genetic, molecular, and cell-biological knowledge on RNS comes from model legumes that exhibit a root-hair mode of bacterial infection, in contrast to the Dalbergoid legumes exhibiting crack-entry of rhizobia. As a step toward understanding this important group of legumes, we have combined microscopic analysis and temporal transcriptome to obtain a dynamic view of plant gene expression during Arachis hypogaea (peanut) nodule development. We generated comprehensive transcriptome data by mapping the reads to A. hypogaea, and two diploid progenitor genomes. Additionally, we performed BLAST searches to identify nodule-induced yet-to-be annotated peanut genes. Comparison between peanut, Medicago truncatula, Lotus japonicus, and Glycine max showed upregulation of 61 peanut orthologs among 111 tested known RNS-related genes, indicating conservation in mechanisms of nodule development among members of the Papilionoid family. Unlike model legumes, recruitment of class 1 phytoglobin-derived symbiotic hemoglobin (SymH) in peanut indicates diversification of oxygen-scavenging mechanisms in the Papilionoid family. Finally, the absence of cysteine-rich motif-1-containing nodule-specific cysteine-rich peptide (NCR) genes but the recruitment of defensin-like NCRs suggest a diverse molecular mechanism of terminal bacteroid differentiation. In summary, our work describes genetic conservation and diversification in legume–rhizobia symbiosis in the Papilionoid family, as well as among members of the Dalbergoid legumes.[Graphic: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license. |
| first_indexed | 2024-12-17T00:58:21Z |
| format | Article |
| id | doaj.art-bbe4f46a390b4abdb9b4e303be2d2eca |
| institution | Directory Open Access Journal |
| issn | 0894-0282 1943-7706 |
| language | English |
| last_indexed | 2024-12-17T00:58:21Z |
| publishDate | 2022-02-01 |
| publisher | The American Phytopathological Society |
| record_format | Article |
| series | Molecular Plant-Microbe Interactions |
| spelling | doaj.art-bbe4f46a390b4abdb9b4e303be2d2eca2022-12-21T22:09:33ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062022-02-0135213114510.1094/MPMI-05-21-0122-RMicroscopic and Transcriptomic Analyses of Dalbergoid Legume Peanut Reveal a Divergent Evolution Leading to Nod-Factor-Dependent Epidermal Crack-Entry and Terminal Bacteroid DifferentiationBikash Raul0Oindrila Bhattacharjee1Amit Ghosh2Priya Upadhyay3Kunal Tembhare4Ajeet Singh5Tarannum Shaheen6Asim Kumar Ghosh7Ivone Torres-Jerez8Nick Krom9Josh Clevenger10Michael Udvardi11Brian E. Scheffler12Peggy Ozias-Akins13Ravi Datta Sharma14Kaustav Bandyopadhyay15Vineet Gaur16Shailesh Kumar17Senjuti Sinharoy18National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi 110067, IndiaNational Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi 110067, IndiaNational Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi 110067, IndiaNational Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi 110067, IndiaNational Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi 110067, IndiaNational Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi 110067, IndiaNational Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi 110067, IndiaNational Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi 110067, IndiaNoble Research Institute, 2510 Sam Noble Pkwy, Ardmore, OK 73401, U.S.A.Noble Research Institute, 2510 Sam Noble Pkwy, Ardmore, OK 73401, U.S.A.University of Georgia, Institute of Plant Breeding, Genetics and Genomics and Department of Horticulture, Tifton, GA 31793, U.S.A.Noble Research Institute, 2510 Sam Noble Pkwy, Ardmore, OK 73401, U.S.A.United States Department of Agriculture–Agricultural Research Service Jamie Whitten Delta States Research Center (JWDSRC) Stoneville, JWDSRC, Bldg.1, Room 229, Experiment Station Road, PO Box 36, Stoneville, MS 38776-0036, U.S.A.University of Georgia, Institute of Plant Breeding, Genetics and Genomics and Department of Horticulture, Tifton, GA 31793, U.S.A.Amity University Haryana, Amity Education Valley, Manesar, Panchgaon, Haryana 122412, IndiaAmity University Haryana, Amity Education Valley, Manesar, Panchgaon, Haryana 122412, IndiaNational Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi 110067, IndiaNational Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi 110067, IndiaNational Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi 110067, IndiaRoot nodule symbiosis (RNS) is the pillar behind sustainable agriculture and plays a pivotal role in the environmental nitrogen cycle. Most of the genetic, molecular, and cell-biological knowledge on RNS comes from model legumes that exhibit a root-hair mode of bacterial infection, in contrast to the Dalbergoid legumes exhibiting crack-entry of rhizobia. As a step toward understanding this important group of legumes, we have combined microscopic analysis and temporal transcriptome to obtain a dynamic view of plant gene expression during Arachis hypogaea (peanut) nodule development. We generated comprehensive transcriptome data by mapping the reads to A. hypogaea, and two diploid progenitor genomes. Additionally, we performed BLAST searches to identify nodule-induced yet-to-be annotated peanut genes. Comparison between peanut, Medicago truncatula, Lotus japonicus, and Glycine max showed upregulation of 61 peanut orthologs among 111 tested known RNS-related genes, indicating conservation in mechanisms of nodule development among members of the Papilionoid family. Unlike model legumes, recruitment of class 1 phytoglobin-derived symbiotic hemoglobin (SymH) in peanut indicates diversification of oxygen-scavenging mechanisms in the Papilionoid family. Finally, the absence of cysteine-rich motif-1-containing nodule-specific cysteine-rich peptide (NCR) genes but the recruitment of defensin-like NCRs suggest a diverse molecular mechanism of terminal bacteroid differentiation. In summary, our work describes genetic conservation and diversification in legume–rhizobia symbiosis in the Papilionoid family, as well as among members of the Dalbergoid legumes.[Graphic: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/MPMI-05-21-0122-RArachis hypogaeabacteria–plant symbiosisbacteroidcrack entryDalbergoid legumesnitrogen fixation |
| spellingShingle | Bikash Raul Oindrila Bhattacharjee Amit Ghosh Priya Upadhyay Kunal Tembhare Ajeet Singh Tarannum Shaheen Asim Kumar Ghosh Ivone Torres-Jerez Nick Krom Josh Clevenger Michael Udvardi Brian E. Scheffler Peggy Ozias-Akins Ravi Datta Sharma Kaustav Bandyopadhyay Vineet Gaur Shailesh Kumar Senjuti Sinharoy Microscopic and Transcriptomic Analyses of Dalbergoid Legume Peanut Reveal a Divergent Evolution Leading to Nod-Factor-Dependent Epidermal Crack-Entry and Terminal Bacteroid Differentiation Molecular Plant-Microbe Interactions Arachis hypogaea bacteria–plant symbiosis bacteroid crack entry Dalbergoid legumes nitrogen fixation |
| title | Microscopic and Transcriptomic Analyses of Dalbergoid Legume Peanut Reveal a Divergent Evolution Leading to Nod-Factor-Dependent Epidermal Crack-Entry and Terminal Bacteroid Differentiation |
| title_full | Microscopic and Transcriptomic Analyses of Dalbergoid Legume Peanut Reveal a Divergent Evolution Leading to Nod-Factor-Dependent Epidermal Crack-Entry and Terminal Bacteroid Differentiation |
| title_fullStr | Microscopic and Transcriptomic Analyses of Dalbergoid Legume Peanut Reveal a Divergent Evolution Leading to Nod-Factor-Dependent Epidermal Crack-Entry and Terminal Bacteroid Differentiation |
| title_full_unstemmed | Microscopic and Transcriptomic Analyses of Dalbergoid Legume Peanut Reveal a Divergent Evolution Leading to Nod-Factor-Dependent Epidermal Crack-Entry and Terminal Bacteroid Differentiation |
| title_short | Microscopic and Transcriptomic Analyses of Dalbergoid Legume Peanut Reveal a Divergent Evolution Leading to Nod-Factor-Dependent Epidermal Crack-Entry and Terminal Bacteroid Differentiation |
| title_sort | microscopic and transcriptomic analyses of dalbergoid legume peanut reveal a divergent evolution leading to nod factor dependent epidermal crack entry and terminal bacteroid differentiation |
| topic | Arachis hypogaea bacteria–plant symbiosis bacteroid crack entry Dalbergoid legumes nitrogen fixation |
| url | https://apsjournals.apsnet.org/doi/10.1094/MPMI-05-21-0122-R |
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