Advances in Multi-Omics Approaches for Molecular Breeding of Black Rot Resistance in Brassica oleracea L

Abstract

Brassica oleracea is one of the most important species of the Brassicaceae family encompassing several economically important vegetables produced and consumed worldwide. But its sustainability is challenged by a range of pathogens, among which black rot, caused by Xanthomonas campestris pv. campestris (Xcc), is the most serious and destructive seed borne bacterial disease, causing huge yield losses. Host-plant resistance could act as the most effective and efficient solution to curb black rot disease for sustainable production of B. oleracea. Recently, 'omics' technologies have emerged as promising tools to understand the host-pathogen interactions, thereby gaining a deeper insight into the resistance mechanisms. In this review, we have summarized the recent achievements made in the emerging omics technologies to tackle the black rot challenge in B. oleracea. With an integrated approach of the omics technologies such as genomics, proteomics, transcriptomics, and metabolomics, it would allow better understanding of the complex molecular mechanisms underlying black rot resistance. Due to the availability of sequencing data, genomics and transcriptomics have progressed as expected for black rot resistance, however, other omics approaches like proteomics and metabolomics are lagging behind, necessitating a holistic and targeted approach to address the complex questions of Xcc-Brassica interactions. Genomic studies revealed that the black rot resistance is a complex trait and is mostly controlled by quantitative trait locus (QTL) with minor effects. Transcriptomic analysis divulged the genes related to photosynthesis, glucosinolate biosynthesis and catabolism, phenylpropanoid biosynthesis pathway, ROS scavenging, calcium signalling, hormonal synthesis and signalling pathway are being differentially expressed upon Xcc infection. Comparative proteomic analysis in relation to susceptible and/or resistance interactions with Xcc identified the involvement of proteins related to photosynthesis, protein biosynthesis, processing and degradation, energy metabolism, innate immunity, redox homeostasis, and defence response and signalling pathways in Xcc-Brassica interaction. Specifically, most of the studies focused on the regulation of the photosynthesis-related proteins as a resistance response in both early and later stages of infection. Metabolomic studies suggested that glucosinolates (GSLs), especially aliphatic and indolic GSLs, its subsequent hydrolysis products, and defensive metabolites synthesized by jasmonic acid (JA)-mediated phenylpropanoid biosynthesis pathway are involved in disease resistance mechanisms against Xcc in Brassica species. Multi-omics analysis showed that JA signalling pathway is regulating resistance against hemibiotrophic pathogen like Xcc. So, the bonhomie between omics technologies and plant breeding is going to trigger major breakthroughs in the field of crop improvement by developing superior cultivars with broad-spectrum resistance. If multi-omics tools are implemented at the right scale, we may be able to achieve the maximum benefits from the minimum. In this review, we have also discussed the challenges, future prospects, and the way forward in the application of omics technologies to accelerate the breeding of B. oleracea for disease resistance. A deeper insight about the current knowledge on omics can offer promising results in the breeding of high-quality disease-resistant crops.

Keywords: Brassica oleracea; Xanthomonas campestris pv. campestris; black rot; genomics; metabolomics; omics; proteomics; transcriptomics.

FIGURE 1

The application of ‘multi-omics’ technologies to develop Xcc resistant B. oleracea and to understand the mechanisms of disease resistance.

FIGURE 2

Different Brassica oleracea varieties infested with Xanthomonas campestris pv. campestris [(A) Cauliflower plants with severe Xcc infection, (B) Broccoli plants with typical symptoms of Xcc, (C) Cabbage plants with heavy Xcc infestation (D) Cauliflower leaves with characteristic V-shaped lesion caused by Xcc infection].

FIGURE 3

A model outlining the R-gene-mediated signalling to (A) induce effector-triggered immunity (ETI) and (B) disease susceptibility upon Xcc inoculation in Brassica napus as proposed by Mamun et al. (2020). JA, jasmonic acid; SA, salicylic acid; CaM, calmodulin; CAS, calcium-sensing receptor; NPR1, non-expressor of pathogenesis-related gene 1; NPR3, non-expressor of pathogenesis-related genes 3; NPR4, non-expressor of pathogenesis-related genes 4; LOX2, lipoxygenase 2; CDPK5, calcium-dependent protein kinase 5; CBP60g, calcium-sensing protein 60 g.

FIGURE 4

Schematic view of a model depicting Jasmonic acid (JA)-mediated phenylpropanoid biosynthesis pathway and hormonal regulations of phenolic accumulation (soluble and cell-wall bound) in relation to resistance against Xcc in Brassica napus adopted from previous studies (Islam et al., 2018, 2019b). JA, jasmonic acid; SA, salicylic acid; ABA, abscisic acid; CK, cytokinin; IAA, indoleacetic acid; MYB TF, MYB transcriptional factor; PAP1, production of anthocyanin pigment 1; PAL, phenylalanine ammonia-lyase; C4H, cinnamate-4-hydroxylase; 4CL, 4-coumaroyl CoA-ligase; CHS, chalcone synthase; CHI, chalcone isomerase; F3H, flavanone 3- hydroxylase; F3’5’H, flavonoid 3’,5’hydroxylase; DFR, dihydroflavanol 4-reductase; ANS, anthocyanidin synthase; ANR, anthocyanidin-reductase; ECGT, epicatechin:1-O-galloyl-β-D-glucose-O-galloyltransferase; HCT, hydroxycinnamoyl-CoA:shikimate hydroxycinnamoyl transferase; C3H, coumarate 3-hydroxylase; CCR, cinnamyl CoA reductase; COMT, caffeic acid O methyltransferase; ALDH, aldehyde dehydrogenase; F5H, ferulate 5- hydroxylase; CAD, cinnamyl alcohol dehydrogenase; GPOD, guaiacol peroxidases; CPOD, coniferyl alcohol peroxidase; PPO, polyphenol oxidase.

FIGURE 5

Schematic diagram representing key genes and pathways involved in Xcc resistance in Brassica species.