Recent Advances in Mechanisms of Plant Defense to Sclerotinia sclerotiorum

Abstract

Sclerotinia sclerotiorum (Lib.) de Bary is an unusual pathogen which has the broad host range, diverse infection modes, and potential double feeding lifestyles of both biotroph and necrotroph. It is capable of infecting over 400 plant species found worldwide and more than 60 names have agriculturally been used to refer to diseases caused by this pathogen. Plant defense to S. sclerotiorum is a complex biological process and exhibits a typical quantitative disease resistance (QDR) response. Recent studies using Arabidopsis thaliana and crop plants have obtained new advances in mechanisms used by plants to cope with S. sclerotiorum infection. In this review, we focused on our current understanding on plant defense mechanisms against this pathogen, and set up a model for the defense process including three stages: recognition of this pathogen, signal transduction and defense response. We also have a particular interest in defense signaling mediated by diverse signaling molecules. We highlight the current challenges and unanswered questions in both the defense process and defense signaling. Essentially, we discussed candidate resistance genes newly mapped by using high-throughput experiments in important crops, and classified these potential gene targets into different stages of the defense process, which will broaden our understanding of the genetic architecture underlying quantitative resistance to S. sclerotiorum. We proposed that more powerful mapping population(s) will be required for accurate and reliable QDR gene identification.

Keywords: Sclerotinia sclerotiorum; candidate resistance genes; genome-wide association study; plant defense; quantitative resistance; signaling molecules.

Figure 1

Schematic model of plant innate immune defense process against Sclerotinia sclerotiorum infection. In the model, plant defense process can be split into (I) recognition, (II) signal-transduction, and (III) defense response. (I) Plant recognition of MAMPs (or PAMPs) and DAMPs are detected by PRRs in apoplast. The SCFE1–RLP30/SOBIR1/BAK1 recognition, a classical PAMP–PRR recognition mode, is shown. PRRs of other MAMPs and the recognition of OGs, typical DAMPs, by WAK1 remain to be identified. Additionally, potential effectors secreted by S. sclerotiorum may recognized by potential NBS-LRRs R protein in cytoplasm. (II) The signal-transduction is performed by the MAP kinase cascade or MAPK-independent pathways. In response to S. sclerotiorum infection, the MAPK-independent pathways, such as calcium (Ca) signaling pathway, are also involved. In the Ca signaling pathway, firstly the NC may be activated by unknown PAMP(s) to produce cAMP and cGMP. Subsequently, the two cyclic nucleotides activate Ca²⁺ channels such as CNGCs, resulting in a Ca²⁺ elevation in the cytoplasm. Then the signal of the cytosolic Ca²⁺ elevation is transduced by Ca²⁺ sensor proteins, such as CaMs, CDPKs as well as CRKs. Further, CDPKs phosphorylate and activate RBOHD/F, resulting in ROS accumulation. However, substrates of CRKs are not yet identified under the pathogen infection. Importantly, many signal molecules, including SA, JA, ET, auxin, ABA, NO as well as ROS, play key roles in the signal-transduction. (III) These signals direct various nuclear proteins including transcription factors, transcription activators as well as protein kinases, such as WRKY33, CAMTA3 and CCaMK, to activate specific defense responses, including pathogenesis-related proteins, ROS production, detoxification, oxidative protection, callose deposition camalexin production and other specialized secondary metabolites. Partition of the defense process is generally according to the ref. (Corwin and Kliebenstein, 2017), and the model is expounded in the following text. PR1, pathogenesis-related protein1; MAMPs, microbial associated molecular patterns; DAMPs, damage-associated molecular patterns; PG, polygalacturonases; RLPs, receptor-like proteins; BAK1, BR insensitive1-associated receptor kinase1; SOBIR1, suppressor of BIR1 BIR1-1; WAK1, wall-associated kinase 1; RLK, receptor-like kinase; BIK1, Botrytis-induced kinase1; NBS-LRR, nucleotide-binding site-leucinerich repeat; MAPK, mitogen activated protein kinase; MAPKKKs, MAPK kinase kinases; MAPKKs, MAPK kinases; MKS1, MPK4 substrate 1; SA, salicylate; JAs, jasmonates; ET, ethylene; EIN2, ethylene insensitive 2; ABA, abscisic acid; NO, nitric oxide; NPR1, nonexpressor of PR1; COI1, the coronatine- insensitive protein 1, and MED16, mediator complex subunit; NC, nucleotidyl cyclase; CNGC, cyclic nucleotide gated channel; ATP, adenosine triphosphate; GTP, guanosine triphosphate; cAMP, cyclic adenosine monophosphate; cGMP, cyclic guanosine monophosphate; NC, nucleotidyl cyclase; CaM, calmodulin; CDPK, calcium-dependent protein kinase; CRK, CDPK-related kinase; RBOH, respiratory burst oxidase homologue; SOD, superoxide dismutase; CCaMK, Ca and CaM-dependent protein kinase; CAMTA3, CaM-binding transcription activator3.