A Genome-Wide Association Study on the Seedless Phenotype in Banana (Musa spp.) Reveals the Potential of a Selected Panel to Detect Candidate Genes in a Vegetatively Propagated Crop

Abstract

Banana (Musa sp.) is a vegetatively propagated, low fertility, potentially hybrid and polyploid crop. These qualities make the breeding and targeted genetic improvement of this crop a difficult and long process. The Genome-Wide Association Study (GWAS) approach is becoming widely used in crop plants and has proven efficient to detecting candidate genes for traits of interest, especially in cereals. GWAS has not been applied yet to a vegetatively propagated crop. However, successful GWAS in banana would considerably help unravel the genomic basis of traits of interest and therefore speed up this crop improvement. We present here a dedicated panel of 105 accessions of banana, freely available upon request, and their corresponding GBS data. A set of 5,544 highly reliable markers revealed high levels of admixture in most accessions, except for a subset of 33 individuals from Papua. A GWAS on the seedless phenotype was then successfully applied to the panel. By applying the Mixed Linear Model corrected for both kinship and structure as implemented in TASSEL, we detected 13 candidate genomic regions in which we found a number of genes potentially linked with the seedless phenotype (i.e. parthenocarpy combined with female sterility). An additional GWAS performed on the unstructured Papuan subset composed of 33 accessions confirmed six of these regions as candidate. Out of both sets of analyses, one strong candidate gene for female sterility, a putative orthologous gene to Histidine Kinase CKI1, was identified. The results presented here confirmed the feasibility and potential of GWAS when applied to small sets of banana accessions, at least for traits underpinned by a few loci. As phenotyping in banana is extremely space and time-consuming, this latest finding is of particular importance in the context of banana improvement.

Plant genetic resources for food and agriculture: opportunities and challenges emerging from the science and information technology revolution

“…Access to large-scale sequence and phenotype information at unprecedented scales is providing new opportunities to accelerate the application of basic research. This includes the ability to formulate testable hypotheses about the genetic architecture of quantitative variation, the genes and biological pathways involved, and the causal variants responsible for the inheritance of complex traits in diverse species (Hamblin et al, 2011;Lipka et al, 2015;Sardos et al, 2016;Yano et al, 2016). It should be noted that raw sequence information, if it is to be correctly interpreted and exploited, needs to be integrated with an intimate knowledge of the biology of the species under consideration, the phenotype or performance of the individuals or population that has been sequenced, and the agro-ecosystem in which they have been grown, including the cultural context and farmers' management practices.…”

Identification of potential gene‐associated major traits using GBS‐GWAS for Korean apple germplasm collections

“…Indeed, Sardos et al. () observed the challenges in generating precise GWAS results in their study on banana. Thus, an accurate method of investigation in a suitable time and having many cumulative phenotype data about the necessary trait are critical for obtaining reliable GWAS results.…”

“…Moreover, differences in the trait estimation method and environmental factors affecting the fruits give rise to uneven phenotype data, which result in drastic deviation among samples (Migicovsky et al, 2016), leading to data not being accumulated and being of poor quality and quantity. Indeed, Sardos et al (2016) observed the challenges in generating precise GWAS results in their study on banana. Thus, an accurate method of investigation in a suitable time and having many cumulative phenotype data about the necessary trait are critical for obtaining reliable GWAS results.…”

“…GWAS of the wood property and male strobili of an unrelated tree species, Cryptomeria japonica D. Don, has been attempted (Uchiyama et al, 2013). Recently, the seedless phenotype of banana was analysed by GWAS at Cornell University (Sardos et al, 2016), and the Japanese pear and nine major traits were dissected for potential testing by GWAS in Rosaceae fruit . In the case of apples, target traits were analysed and several associated genes were confirmed by Khan, Olsen, Sovero, Kushad, and Korban (2014) and Migicovsky et al (2016), using GWAS on many traits through collecting and arranging previously accumulated phenotype data.…”

Translating the “Banana Genome” to Delineate Stress Resistance, Dwarfing, Parthenocarpy and Mechanisms of Fruit Ripening

“…Genetically, parthenocarpy may happen due to a single partially dominant gene as in cucurbits (Kim et al, 1992; Menezes et al, 2005) or due to a single recessive gene as in sweet pepper (Tiwari et al, 2011) or due pleiotropy of major and minor genes as in brinjal/eggplant (Miyatake et al, 2012). In case of banana, parthenocarpy is hypothesized (Sardos et al, 2016) to be due to a major dominant gene ( P or P1 ) interacting with minor ones (Simmonds, 1953). With decoding of structural genome of banana, discovery of the precise mechanism of parthenocarpy will give a boost to quality fruit production in commercial plantation.…”