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The genomes of 5 underutilized Papilionoideae crops provide insights into root nodulation and disease resistance
Abstract Background The Papilionoideae subfamily contains a large amount of underutilized legume crops, which are important for food security and human sustainability. However, the lack of genomic resources has hindered the breeding and utilization of these crops. Results Here, we present chromosome...
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description | Abstract
Background
The Papilionoideae subfamily contains a large amount of underutilized legume crops, which are important for food security and human sustainability. However, the lack of genomic resources has hindered the breeding and utilization of these crops.
Results
Here, we present chromosome-level reference genomes for 5 underutilized diploid Papilionoideae crops: sword bean (Canavalia gladiata), scarlet runner bean (Phaseolus coccineus), winged bean (Psophocarpus tetragonolobus), smooth rattlebox (Crotalaria pallida), and butterfly pea (Clitoria ternatea), with assembled genome sizes of 0.62 Gb, 0.59 Gb, 0.71 Gb, 1.22 Gb, and 1.72 Gb, respectively. We found that the long period of higher long terminal repeat retrotransposon activity is the major reason that the genome size of smooth rattlebox and butterfly pea is enlarged. Additionally, there have been no recent whole-genome duplication (WGD) events in these 5 species except for the shared papilionoid-specific WGD event (∼55 million years ago). Then, we identified 5,328 and 10,434 species-specific genes between scarlet runner bean and common bean, respectively, which may be responsible for their phenotypic and functional differences and species-specific functions. Furthermore, we identified the key genes involved in root-nodule symbiosis (RNS) in all 5 species and found that the NIN gene was duplicated in the early Papilionoideae ancestor, followed by the loss of 1 gene copy in smooth rattlebox and butterfly pea lineages. Last, we identified the resistance (R) genes for plant defenses in these 5 species and characterized their evolutionary history.
Conclusions
In summary, this study provides chromosome-scale reference genomes for 3 grain and vegetable beans (sword bean, scarlet runner bean, winged bean), along with genomes for a green manure crop (smooth rattlebox) and a food dyeing crop (butterfly pea). These genomes are crucial for studying phylogenetic history, unraveling nitrogen-fixing RNS evolution, and advancing plant defense research. |
doi_str_mv | 10.1093/gigascience/giae063 |
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Background
The Papilionoideae subfamily contains a large amount of underutilized legume crops, which are important for food security and human sustainability. However, the lack of genomic resources has hindered the breeding and utilization of these crops.
Results
Here, we present chromosome-level reference genomes for 5 underutilized diploid Papilionoideae crops: sword bean (Canavalia gladiata), scarlet runner bean (Phaseolus coccineus), winged bean (Psophocarpus tetragonolobus), smooth rattlebox (Crotalaria pallida), and butterfly pea (Clitoria ternatea), with assembled genome sizes of 0.62 Gb, 0.59 Gb, 0.71 Gb, 1.22 Gb, and 1.72 Gb, respectively. We found that the long period of higher long terminal repeat retrotransposon activity is the major reason that the genome size of smooth rattlebox and butterfly pea is enlarged. Additionally, there have been no recent whole-genome duplication (WGD) events in these 5 species except for the shared papilionoid-specific WGD event (∼55 million years ago). Then, we identified 5,328 and 10,434 species-specific genes between scarlet runner bean and common bean, respectively, which may be responsible for their phenotypic and functional differences and species-specific functions. Furthermore, we identified the key genes involved in root-nodule symbiosis (RNS) in all 5 species and found that the NIN gene was duplicated in the early Papilionoideae ancestor, followed by the loss of 1 gene copy in smooth rattlebox and butterfly pea lineages. Last, we identified the resistance (R) genes for plant defenses in these 5 species and characterized their evolutionary history.
Conclusions
In summary, this study provides chromosome-scale reference genomes for 3 grain and vegetable beans (sword bean, scarlet runner bean, winged bean), along with genomes for a green manure crop (smooth rattlebox) and a food dyeing crop (butterfly pea). These genomes are crucial for studying phylogenetic history, unraveling nitrogen-fixing RNS evolution, and advancing plant defense research.</description><identifier>ISSN: 2047-217X</identifier><identifier>EISSN: 2047-217X</identifier><identifier>DOI: 10.1093/gigascience/giae063</identifier><identifier>PMID: 39190925</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Beans ; Canavalia gladiata ; Chromosomes ; Clitoria ternatea ; Crops ; Crops, Agricultural - genetics ; Crotalaria pallida ; Data Note ; Defense mechanisms ; Diploids ; Disease resistance ; Disease Resistance - genetics ; Evolutionary genetics ; Fabaceae - genetics ; Food dyes ; Food security ; Functionals ; Genes ; Genome Size ; Genome, Plant ; Genomes ; Genomics - methods ; Legumes ; Long terminal repeat ; Nitrogen fixation ; Nitrogenation ; Nodulation ; Papilionoideae ; Peas ; Phaseolus coccineus ; Phylogeny ; Plant breeding ; Plant Diseases - genetics ; Plant Root Nodulation - genetics ; Psophocarpus tetragonolobus ; Species ; Symbiosis ; Winged beans</subject><ispartof>Gigascience, 2024-01, Vol.13</ispartof><rights>The Author(s) 2024. Published by Oxford University Press GigaScience. 2024</rights><rights>The Author(s) 2024. Published by Oxford University Press GigaScience.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c353t-db7f6e44866698661f83bbd9c3c85a821c53dc19cb7fbf58cea33fe9f67258903</cites><orcidid>0000-0001-5036-8733 ; 0000-0002-8754-4195 ; 0000-0001-9367-2524 ; 0000-0002-2524-7523 ; 0000-0001-5518-9662 ; 0009-0008-6440-1643 ; 0000-0002-5536-5475 ; 0000-0003-1359-0970</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11348429/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11348429/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,1598,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39190925$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yuan, Lihua</creatorcontrib><creatorcontrib>Lei, Lihong</creatorcontrib><creatorcontrib>Jiang, Fan</creatorcontrib><creatorcontrib>Wang, Anqi</creatorcontrib><creatorcontrib>Chen, Rong</creatorcontrib><creatorcontrib>Wang, Hengchao</creatorcontrib><creatorcontrib>Meng, Sihan</creatorcontrib><creatorcontrib>Fan, Wei</creatorcontrib><title>The genomes of 5 underutilized Papilionoideae crops provide insights into root nodulation and disease resistance</title><title>Gigascience</title><addtitle>Gigascience</addtitle><description>Abstract
Background
The Papilionoideae subfamily contains a large amount of underutilized legume crops, which are important for food security and human sustainability. However, the lack of genomic resources has hindered the breeding and utilization of these crops.
Results
Here, we present chromosome-level reference genomes for 5 underutilized diploid Papilionoideae crops: sword bean (Canavalia gladiata), scarlet runner bean (Phaseolus coccineus), winged bean (Psophocarpus tetragonolobus), smooth rattlebox (Crotalaria pallida), and butterfly pea (Clitoria ternatea), with assembled genome sizes of 0.62 Gb, 0.59 Gb, 0.71 Gb, 1.22 Gb, and 1.72 Gb, respectively. We found that the long period of higher long terminal repeat retrotransposon activity is the major reason that the genome size of smooth rattlebox and butterfly pea is enlarged. Additionally, there have been no recent whole-genome duplication (WGD) events in these 5 species except for the shared papilionoid-specific WGD event (∼55 million years ago). Then, we identified 5,328 and 10,434 species-specific genes between scarlet runner bean and common bean, respectively, which may be responsible for their phenotypic and functional differences and species-specific functions. Furthermore, we identified the key genes involved in root-nodule symbiosis (RNS) in all 5 species and found that the NIN gene was duplicated in the early Papilionoideae ancestor, followed by the loss of 1 gene copy in smooth rattlebox and butterfly pea lineages. Last, we identified the resistance (R) genes for plant defenses in these 5 species and characterized their evolutionary history.
Conclusions
In summary, this study provides chromosome-scale reference genomes for 3 grain and vegetable beans (sword bean, scarlet runner bean, winged bean), along with genomes for a green manure crop (smooth rattlebox) and a food dyeing crop (butterfly pea). These genomes are crucial for studying phylogenetic history, unraveling nitrogen-fixing RNS evolution, and advancing plant defense research.</description><subject>Beans</subject><subject>Canavalia gladiata</subject><subject>Chromosomes</subject><subject>Clitoria ternatea</subject><subject>Crops</subject><subject>Crops, Agricultural - genetics</subject><subject>Crotalaria pallida</subject><subject>Data Note</subject><subject>Defense mechanisms</subject><subject>Diploids</subject><subject>Disease resistance</subject><subject>Disease Resistance - genetics</subject><subject>Evolutionary genetics</subject><subject>Fabaceae - genetics</subject><subject>Food dyes</subject><subject>Food security</subject><subject>Functionals</subject><subject>Genes</subject><subject>Genome Size</subject><subject>Genome, Plant</subject><subject>Genomes</subject><subject>Genomics - methods</subject><subject>Legumes</subject><subject>Long terminal repeat</subject><subject>Nitrogen fixation</subject><subject>Nitrogenation</subject><subject>Nodulation</subject><subject>Papilionoideae</subject><subject>Peas</subject><subject>Phaseolus coccineus</subject><subject>Phylogeny</subject><subject>Plant breeding</subject><subject>Plant Diseases - genetics</subject><subject>Plant Root Nodulation - genetics</subject><subject>Psophocarpus tetragonolobus</subject><subject>Species</subject><subject>Symbiosis</subject><subject>Winged beans</subject><issn>2047-217X</issn><issn>2047-217X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><recordid>eNqNkU9rHSEUxaWkJCHNJygUIZtsXqrj_NFVCaFNCoF2kUJ34uideYZ5OvU6gfTT1_BewmtWcaFH_N3j1UPIR84uOFPi8-hHg9ZDsFC0AdaKd-S4YnW3qnj3-2BPH5FTxHtWRtdJ2YlDciQUV0xVzTGZ79ZARwhxA0jjQBu6BAdpyX7yf8HRn2YuKoboHRigNsUZ6ZziQ9lTH9CP64xF5EhTjJmG6JbJ5FJBTXDUeQSDQBOgx2xKtx_I-8FMCKe79YT8-vb17upmdfvj-vvV5e3Kikbkleu7oYW6lm3bqjLxQYq-d8oKKxsjK24b4SxXtnD90EgLRogB1NB2VSMVEyfky9Z3XvoNOAshJzPpOfmNSY86Gq__Pwl-rcf4oDkXtawrVRzOdw4p_lkAs954tDBNJkBcUAumOtkwWT9ddvYKvY9LCuV9WnAmWKHaqlBiS5VfREwwvHTDmX5KVe-lqneplqpP-w95qXnOsAAXWyAu85sc_wHns7V2</recordid><startdate>20240102</startdate><enddate>20240102</enddate><creator>Yuan, Lihua</creator><creator>Lei, Lihong</creator><creator>Jiang, Fan</creator><creator>Wang, Anqi</creator><creator>Chen, Rong</creator><creator>Wang, Hengchao</creator><creator>Meng, Sihan</creator><creator>Fan, Wei</creator><general>Oxford University Press</general><scope>TOX</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>JQ2</scope><scope>K9.</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5036-8733</orcidid><orcidid>https://orcid.org/0000-0002-8754-4195</orcidid><orcidid>https://orcid.org/0000-0001-9367-2524</orcidid><orcidid>https://orcid.org/0000-0002-2524-7523</orcidid><orcidid>https://orcid.org/0000-0001-5518-9662</orcidid><orcidid>https://orcid.org/0009-0008-6440-1643</orcidid><orcidid>https://orcid.org/0000-0002-5536-5475</orcidid><orcidid>https://orcid.org/0000-0003-1359-0970</orcidid></search><sort><creationdate>20240102</creationdate><title>The genomes of 5 underutilized Papilionoideae crops provide insights into root nodulation and disease resistance</title><author>Yuan, Lihua ; Lei, Lihong ; Jiang, Fan ; Wang, Anqi ; Chen, Rong ; Wang, Hengchao ; Meng, Sihan ; Fan, Wei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c353t-db7f6e44866698661f83bbd9c3c85a821c53dc19cb7fbf58cea33fe9f67258903</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Beans</topic><topic>Canavalia gladiata</topic><topic>Chromosomes</topic><topic>Clitoria ternatea</topic><topic>Crops</topic><topic>Crops, Agricultural - genetics</topic><topic>Crotalaria pallida</topic><topic>Data Note</topic><topic>Defense mechanisms</topic><topic>Diploids</topic><topic>Disease resistance</topic><topic>Disease Resistance - genetics</topic><topic>Evolutionary genetics</topic><topic>Fabaceae - genetics</topic><topic>Food dyes</topic><topic>Food security</topic><topic>Functionals</topic><topic>Genes</topic><topic>Genome Size</topic><topic>Genome, Plant</topic><topic>Genomes</topic><topic>Genomics - methods</topic><topic>Legumes</topic><topic>Long terminal repeat</topic><topic>Nitrogen fixation</topic><topic>Nitrogenation</topic><topic>Nodulation</topic><topic>Papilionoideae</topic><topic>Peas</topic><topic>Phaseolus coccineus</topic><topic>Phylogeny</topic><topic>Plant breeding</topic><topic>Plant Diseases - genetics</topic><topic>Plant Root Nodulation - genetics</topic><topic>Psophocarpus tetragonolobus</topic><topic>Species</topic><topic>Symbiosis</topic><topic>Winged beans</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yuan, Lihua</creatorcontrib><creatorcontrib>Lei, Lihong</creatorcontrib><creatorcontrib>Jiang, Fan</creatorcontrib><creatorcontrib>Wang, Anqi</creatorcontrib><creatorcontrib>Chen, Rong</creatorcontrib><creatorcontrib>Wang, Hengchao</creatorcontrib><creatorcontrib>Meng, Sihan</creatorcontrib><creatorcontrib>Fan, Wei</creatorcontrib><collection>Open Access: Oxford University Press Open Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Gigascience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yuan, Lihua</au><au>Lei, Lihong</au><au>Jiang, Fan</au><au>Wang, Anqi</au><au>Chen, Rong</au><au>Wang, Hengchao</au><au>Meng, Sihan</au><au>Fan, Wei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The genomes of 5 underutilized Papilionoideae crops provide insights into root nodulation and disease resistance</atitle><jtitle>Gigascience</jtitle><addtitle>Gigascience</addtitle><date>2024-01-02</date><risdate>2024</risdate><volume>13</volume><issn>2047-217X</issn><eissn>2047-217X</eissn><abstract>Abstract
Background
The Papilionoideae subfamily contains a large amount of underutilized legume crops, which are important for food security and human sustainability. However, the lack of genomic resources has hindered the breeding and utilization of these crops.
Results
Here, we present chromosome-level reference genomes for 5 underutilized diploid Papilionoideae crops: sword bean (Canavalia gladiata), scarlet runner bean (Phaseolus coccineus), winged bean (Psophocarpus tetragonolobus), smooth rattlebox (Crotalaria pallida), and butterfly pea (Clitoria ternatea), with assembled genome sizes of 0.62 Gb, 0.59 Gb, 0.71 Gb, 1.22 Gb, and 1.72 Gb, respectively. We found that the long period of higher long terminal repeat retrotransposon activity is the major reason that the genome size of smooth rattlebox and butterfly pea is enlarged. Additionally, there have been no recent whole-genome duplication (WGD) events in these 5 species except for the shared papilionoid-specific WGD event (∼55 million years ago). Then, we identified 5,328 and 10,434 species-specific genes between scarlet runner bean and common bean, respectively, which may be responsible for their phenotypic and functional differences and species-specific functions. Furthermore, we identified the key genes involved in root-nodule symbiosis (RNS) in all 5 species and found that the NIN gene was duplicated in the early Papilionoideae ancestor, followed by the loss of 1 gene copy in smooth rattlebox and butterfly pea lineages. Last, we identified the resistance (R) genes for plant defenses in these 5 species and characterized their evolutionary history.
Conclusions
In summary, this study provides chromosome-scale reference genomes for 3 grain and vegetable beans (sword bean, scarlet runner bean, winged bean), along with genomes for a green manure crop (smooth rattlebox) and a food dyeing crop (butterfly pea). These genomes are crucial for studying phylogenetic history, unraveling nitrogen-fixing RNS evolution, and advancing plant defense research.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>39190925</pmid><doi>10.1093/gigascience/giae063</doi><orcidid>https://orcid.org/0000-0001-5036-8733</orcidid><orcidid>https://orcid.org/0000-0002-8754-4195</orcidid><orcidid>https://orcid.org/0000-0001-9367-2524</orcidid><orcidid>https://orcid.org/0000-0002-2524-7523</orcidid><orcidid>https://orcid.org/0000-0001-5518-9662</orcidid><orcidid>https://orcid.org/0009-0008-6440-1643</orcidid><orcidid>https://orcid.org/0000-0002-5536-5475</orcidid><orcidid>https://orcid.org/0000-0003-1359-0970</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Beans Canavalia gladiata Chromosomes Clitoria ternatea Crops Crops, Agricultural - genetics Crotalaria pallida Data Note Defense mechanisms Diploids Disease resistance Disease Resistance - genetics Evolutionary genetics Fabaceae - genetics Food dyes Food security Functionals Genes Genome Size Genome, Plant Genomes Genomics - methods Legumes Long terminal repeat Nitrogen fixation Nitrogenation Nodulation Papilionoideae Peas Phaseolus coccineus Phylogeny Plant breeding Plant Diseases - genetics Plant Root Nodulation - genetics Psophocarpus tetragonolobus Species Symbiosis Winged beans |
title | The genomes of 5 underutilized Papilionoideae crops provide insights into root nodulation and disease resistance |
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