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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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Published in:Gigascience 2024-01, Vol.13
Main Authors: Yuan, Lihua, Lei, Lihong, Jiang, Fan, Wang, Anqi, Chen, Rong, Wang, Hengchao, Meng, Sihan, Fan, Wei
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Fan, Wei
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.
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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. 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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). 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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 &amp; 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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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