Molecular and Cellular Mechanisms Involved in Host-Specific Resistance to Cyst Nematodes in Crops

Abstract

Cyst nematodes are able to infect a wide range of crop species and are regarded as a major threat in crop production. In response to invasion of cyst nematodes, plants activate their innate immune system to defend themselves by conferring basal and host-specific defense responses depending on the plant genotype. Basal defense is dependent on the detection of pathogen-associated molecular patterns (PAMPs) by pattern recognition receptors (PRRs), while host-specific defense mainly relies on the activation of canonical and non-canonical resistance (R) genes or quantitative trait loci (QTL). Currently, application of R genes and QTLs in crop species is a major approach to control cyst nematode in crop cultivation. However, emerging virulent cyst nematode field populations are threatening crop production due to host genetic selection by the application of a limited set of resistance genes in current crop cultivars. To counteract this problem, increased knowledge about the mechanisms involved in host-specific resistance mediated by R genes and QTLs to cyst nematodes is indispensable to improve their efficient and sustainable use in field crops. Despite the identification of an increasing number of resistance traits to cyst nematodes in various crops, the underlying genes and defense mechanisms are often unknown. In the last decade, indebt studies on the functioning of a number of cyst nematode R genes and QTLs have revealed novel insights in how plants respond to cyst nematode infection by the activation of host-specific defense responses. This review presents current knowledge of molecular and cellular mechanisms involved in the recognition of cyst nematodes, the activation of defense signaling and resistance response types mediated by R genes or QTLs. Finally, future directions for research are proposed to develop management strategies to better control cyst nematodes in crop cultivation.

Keywords: cyst nematode; effector; host-specific resistance; immune receptor; plant immunity; resistance gene; resistance locus.

Figure 1

Overview of major cyst nematode resistance (R) genes and loci (QTLs) identified in crop species, for which knowledge is available on the molecular and cellular mechanisms underlying cyst nematode resistance. Extracellular immune receptors: Cf-2 from tomato encodes a RLP and confers resistance to the potato cyst nematode (PCN) Globodera rostochiensis, respectively. Cf-2 detects the nematode effector GrVAP-1 via the host factor Rcr3, which is activated by apoplastic serine proteases named subtilases to induce apoplastic immunity. Intracellular Nucleotide binding (NB)-Leucine-rich Repeat (LRR; NLR) immune receptors: Gro1-4 from potato encodes a toll-interleukin receptor-nucleotide binding-LRR (TIR-NB-LRR) protein, whereas Gpa2 from potato encodes a coiled coil-NB-LRR (CC-NB-LRR) protein. Hero A from tomato encodes a Solanaceae Domain-CC-NB-LRR (SD-CC-NB-LRR) protein. These intracellular immune receptors all confer resistance to specific PCN populations from G. rostochiensis, Globodera pallida, or both. Only for Gpa2, the matching nematode effector GpRBP-1 is known which is able to activate a local HR response. Detection of nematode effector GpRBP-1 by Gpa2 requires a host factor RanGAP2. Resistance loci: the Rhg1 and Rhg4 loci from soybean confer resistance to field populations from the cyst nematode Heterodera glycines. Rhg1-mediated resistance depends on copy number variation, as the high copy number Rhg1 type confers resistance on its own while the low copy number Rhg1 type requires the Rhg4 locus to confer resistance. Two polymoriphisms determine Rhg4-mediated resistance.

Figure 2

Host-specific defense responses against cyst nematodes in plant roots harboring major R genes or resistance loci (QTLs). Type I. A subset of R genes mediate early defense responses to cyst nematodes that allows syncytium initiation but restricts further expansion by forming a layer of necrotic cells around the young feeding structures. As a result, these encapsulated syncytia allow the development of males but not females. This “male-biased” resistance is seen for R genes like H1 in potato and Hero A in tomato. Type II. Another subset of R genes mediates a late defense response that allows syncytium formation and expansion, supporting the development of females. In this case, a layer of necrotic cells is formed around the expanded syncytium which disrupts the connection between the syncytium and the vascular cylinder. Thereby, female development is restricted due to the lack of nutrition. This “female-biased” resistance is observed for R genes like Gpa2 from potato. Whereas the type I and II responses are typical for cyst nematode R genes encoding NB-LRR immune receptors, the resistance loci Rhg1 and Rhg4 trigger non-canonical resistance responses to cyst nematodes in soybean roots. Type III. The high copy number Rhg1-b type encodes a α-SNAP protein that poorly interacts with the protein NSF to disrupt vesical trafficking. Meanwhile, the hyperaccumulation of α-SNAP is thought to promote the collapse of the plant-nematode biotrophic interface leading to nematode resistance. Type IV. Rhg4-mediated resistance is determined by two polymorphisms in the encoded protein serine hydroxymethyltransferase (SHMT). SHMT regulates folate homeostasis leading to folate deficiency, causing the poor development and difficult maintenance of syncytia. Interestingly, cross-talk occurs in low copy number Rhg1-a, which requires Rhg-4 to activate SCN resistance. It is thought that the elevated levels of Rhg1-a encoded α-SNAP induces Rhg-4 encoded SHMT, which then physically interact with each other to form a complex with the pathogenesis-related protein PR08-Bet. This multiprotein complex regulates the activity of SHMT which leads to syncytium collapse and thus cyst nematode resistance.