Understanding the Sorghum- Colletotrichum sublineola Interactions for Enhanced Host Resistance

Abstract

Improving sorghum resistance is a sustainable method to reduce yield losses due to anthracnose, a devastating disease caused by Colletotrichum sublineola. Elucidating the molecular mechanisms of sorghum-C. sublineola interactions would help identify biomarkers for rapid and efficient identification of novel sources for host-plant resistance improvement, understanding the pathogen virulence, and facilitating resistance breeding. Despite concerted efforts to identify resistance sources, the knowledge about sorghum-anthracnose interactions remains scanty. Hence, in this review, we presented an overview of the current knowledge on the mechanisms of sorghum-C. sublineola molecular interactions, sources of resistance for sorghum breeding, quantitative trait loci (QTL), and major (R-) resistance gene sequences as well as defense-related genes associated with anthracnose resistance. We summarized current knowledge about C. sublineola populations and its virulence. Illustration of the sorghum-C. sublineola interaction model based on the current understanding is also provided. We highlighted the importance of genomic resources of both organisms for integrated omics research to unravel the key molecular components underpinning compatible and incompatible sorghum-anthracnose interactions. Furthermore, sorghum-breeding strategy employing rapid sorghum germplasm screening, systems biology, and molecular tools is presented.

Keywords: Colletotrichum sublineola; R-genes; anthracnose; germplasm; host-plant resistance; quantitative trait loci; sorghum.

Figure 1

(A) Average production of sorghum in top 10 sorghum producing countries from 1994 to 2018, and (B) corresponding production share by region. Data source (FAOSTAT, 2020). Sudan (former) reflects average sorghum production in Sudan and South Sudan up to 2011. For Sudan, the data represent average production from 2012 to 2018.

Figure 2

Overview of sorghum-Colletotrichum sublineola interactions. Spores of C. sublineola land on sorghum tissue, propagate into germ tubes, and form appressoria, which are specialized infection structures. The infection penetrates the host cell wall (CW) and forms feeding structures called haustoria. During the course of infection, pathogenicity molecules, such as cell wall degrading enzymes (CWDEs) and effectors are secreted into the extracellular space. The CWDEs and ubiquitous structural molecules such as chitin are recognized as Pathogen associated molecular patterns (PAMPs) by the host cell receptors, receptor kinases (RK), and receptor like proteins (RLP). These receptors interacts with extracellular leucine rich repeat (LRR) and intracellular BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) activating the PAMP-triggered immunity (PTI). Host PTI response is characterized by increased accumulation of hydrogen peroxide (H₂O₂), phenolics, phytoalexins, hydroxyprolinerich glycoproteins (HRGPs), pathogenesis- related (PR-) proteins, and callose deposition around the point of infection and suppress pathogen growth. In susceptible genotypes, the pathogen secrets effectors that suppress the PTI whereas in resistant genotypes these extracellular and intracellular effectors are recognized by the host nucleotide-binding (NB) LRR (NB-LRR) receptors. This recognition induces the effector-triggered immunity (ETI) primarily recognized by accumulation of H₂O₂ resulting in hypersensitive response (HR), which is a form of programmed cell death. The ETI response blocks C. sublineola transition to necrotrophic phase and arrests the pathogen growth. Both PTI and ETI responses involve transcriptional factors (green) and phytohormones (gray), involved in signaling transduction, regulation of defense-related genes, and host physiology.

Figure 3

Schematic flow representing a strategy for the development of anthracnose resistant sorghum cultivars through the identification of resistance sources, development and application of biomarkers as well as understanding the pathosystems. Large-scale resistance screening using diverse C. sublineola strains would lead to the identification of resistant and susceptible genotypes. Integrated omics is an efficient approach to identify and characterize compatible (susceptibility) and incompatible (resistance) reaction of sorghum genotypes as well as to identify markers related to plant defense and pathogenicity factors. Availability of genomic information on sorghum and C. sublineola would enable efficient application of integrated omics approach to unravel their interactions. Validated markers for their association with the target trait can facilitate the identification of resistant genotypes in a diverse sorghum germplasm while defense related genes, particularly major R-genes are useful for genetic improvement of sorghum cultivars. However, the ever-evolving pathogen populations continue to pose a challenge to resistant cultivars deployed for production. Hence, it is important to add newly identified resistant cultivars to existing resistance gene pool and frequently re-evaluate their resistance against new C. sublineola strains to ensure durability of the resistance.