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QTL mapping and transcriptome analysis of cowpea reveals candidate genes for root-knot nematode resistance.

ABSTRACT: Cowpea is one of the most important food and forage legumes in drier regions of the tropics and subtropics. However, cowpea yield worldwide is markedly below the known potential due to abiotic and biotic stresses, including parasitism by root-knot nematodes (Meloidogyne spp., RKN). Two resistance genes with dominant effect, Rk and Rk2, have been reported to provide resistance against RKN in cowpea. Despite their description and use in breeding for resistance to RKN and particularly genetic mapping of the Rk locus, the exact genes conferring resistance to RKN remain unknown. In the present work, QTL mapping using recombinant inbred line (RIL) population 524B x IT84S-2049 segregating for a newly mapped locus and analysis of the transcriptome changes in two cowpea near-isogenic lines (NIL) were used to identify candidate genes for Rk and the newly mapped locus. A major QTL, designated QRk-vu9.1, associated with resistance to Meloidogyne javanica reproduction, was detected and mapped on linkage group LG9 at position 13.37 cM using egg production data. Transcriptome analysis on resistant and susceptible NILs 3 and 9 days after inoculation revealed up-regulation of 109 and 98 genes and down-regulation of 110 and 89 genes, respectively, out of 19,922 unique genes mapped to the common bean reference genome. Among the differentially expressed genes, four and nine genes were found within the QRk-vu9.1 and QRk-vu11.1 QTL intervals, respectively. Six of these genes belong to the TIR-NBS-LRR family of resistance genes and three were upregulated at one or more time-points. Quantitative RT-PCR validated gene expression to be positively correlated with RNA-seq expression pattern for eight genes. Future functional analysis of these cowpea genes will enhance our understanding of Rk-mediated resistance and identify the specific gene responsible for the resistance.

SUBMITTER: Santos JRP

PROVIDER: S-EPMC5754085 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe root-knot nematode Meloidogyne graminicola is an obligate biotrophic pathogen considered to be the most damaging nematode species that causes significant yield losses to upland and rainfed lowland rice production in South and Southeast Asia. Mapping and identification of quantitative trait loci (QTL) for resistance to and tolerance for M. graminicola may offer a safe and economic management option to farmers. In this study, resistance to and tolerance for M. graminicola in Asian rice (Oryza sativa L.) were studied in a mapping population consisting of 300 recombinant inbred lines (RILs) derived from IR78877-208-B-1-2, an aerobic rice genotype with improved resistance to and tolerance for M. graminicola, and IR64, a popular, high-yielding rice mega-variety susceptible to M. graminicola. RILs were phenotyped for resistance and tolerance in the dry seasons of 2012 and 2013. QTL analysis was performed using 131 single nucleotide polymorphism (SNP) and 33 simple sequence repeat (SSR) markers.ResultsThree QTLs with main effects on chromosomes 4 (qMGR4.1), 7 (qMGR7.1) and 9 (qMGR9.1) and two epistatic interactions (qMGR3.1/ qMGR11.1 and qMGR4.2/ qMGR8.1) associated with nematode reproduction that were consistent in the two seasons were detected. A QTL affecting root galling was found on chromosomes 4 (qGR4.1) and 8 (qGR8.1), and QTLs for nematode tolerance were found on chromosomes 5 (qYR5.1) and 11 (qYR11.1). These QTLs were consistent in both seasons. A QTL for grain yield was found on chromosome 10 (qGYLD10.1), a QTL affecting filled grains per panicle was detected on chromosome 11 (qFG11.1) and a QTL for fresh root weight was found on chromosomes 2 (qFRWt2.1), 8 (qFRWt8.1) and 12 (qFRWt12.1) in both seasons. The donor of the alleles for qMGR4.1, qMGR7.1, qMGR9.1, qGR4.1, qGR8.1, qYR5.1 and qFRWt2.1 was IR78877-208-B-1-2, whereas for qYR11.1, qGYLD10.1 and qFG11.1, qFRWt8.1 and qFRWt12.1 was IR64. Lines having favorable alleles for resistance, tolerance and yield provided better yield under nematode-infested conditions and could be a starting point of marker-assisted breeding (MAB) for the improvement of M. graminicola resistance and tolerance in Asian rice.ConclusionThis study identified a total of 12 QTLs with main effects and two epistatic interactions in the 1st season and 2nd season related to M. graminicola resistance and tolerance, and other agronomic traits such as plant yield, percentage of filled grains, and fresh and dry root weight. Rice genotypes that have the favorable alleles for resistance (qMGR4.1, qMGR7.1, qMGR9.1, qGR4.1, qGR8.1) and tolerance (qYR5.1, and qYR11.1,) QTLs, and which are either resistant or partially resistant and tolerant, were also selected. These selected genotypes and the identified QTLs are vital information in designing MAB for the improvement of high-yielding rice genotypes but are susceptible to M. graminicola infection.

Project description:Root knot (Meloidogyne spp.) and cyst (Heterodera and Globodera spp.) nematodes infect all important crop species, and the annual economic loss due to these pathogens exceeds $90 billion. We screened the worldwide accession collection with the root-knot nematodes Meloidogyne incognita, M. arenaria and M. hapla, soybean cyst nematode (SCN-Heterodera glycines), sugar beet cyst nematode (SBCN-Heterodera schachtii) and clover cyst nematode (CLCN-Heterodera trifolii), revealing resistant and susceptible accessions. In the over 100 accessions evaluated, we observed a range of responses to the root-knot nematode species, and a non-host response was observed for SCN and SBCN infection. However, variation was observed with respect to infection by CLCN. While many cultivars including Jemalong A17 were resistant to H. trifolii, cultivar Paraggio was highly susceptible. Identification of M. truncatula as a host for root-knot nematodes and H. trifolii and the differential host response to both RKN and CLCN provide the opportunity to genetically and molecularly characterize genes involved in plant-nematode interaction. Accession DZA045, obtained from an Algerian population, was resistant to all three root-knot nematode species and was used for further studies. The mechanism of resistance in DZA045 appears different from Mi-mediated root-knot nematode resistance in tomato. Temporal analysis of nematode infection showed that there is no difference in nematode penetration between the resistant and susceptible accessions, and no hypersensitive response was observed in the resistant accession even several days after infection. However, less than 5% of the nematode population completed the life cycle as females in the resistant accession. The remainder emigrated from the roots, developed as males, or died inside the roots as undeveloped larvae. Genetic analyses carried out by crossing DZA045 with a susceptible French accession, F83005, suggest that one gene controls resistance in DZA045.

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QTL mapping and transcriptome analysis of cowpea reveals candidate genes for root-knot nematode resistance.

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