Resistance to the wheat curl mite and mite-transmitted viruses: challenges and future directions

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Highlights

  • Wheat curl mites are the sole vector for four damaging viruses that impact wheat production.

  • There are limited sources of host genetic resistance to this disease complex.

  • Emerging virulent WCM populations and novel virus isolates highlight the need for more diverse sources of resistance.

  • Genome sequencing will be critical to reveal the full extent of genetic diversity in mite and virus populations.

  • A mechanistic understanding of the pathosystem will help identify and engineer novel resistance alleles.

Wheat curl mite (WCM) is the only known arthropod vector of four wheat viruses, the most important of which is Wheat streak mosaic virus (WSMV). Host resistance to WCM and WSMV is limited to a small number of loci, most of which are introgressed from wild relatives and are often associated with linkage drag and temperature sensitivity. Reports of virulent WCM populations and potential resistance-breaking WSMV isolates highlight the need for more diverse sources of resistance. Genome sequencing will be critical to fully characterize the genetic diversity in WCM and WSMV populations to better understand the incidence of WCM-transmitted viruses and to evaluate the potential stability of resistance genes. Characterizing host resistance genes will help build a mechanistic understanding of wheat-WCM-WSMV interactions and inform strategies to identify and engineer more durable resistance sources.

Introduction

Globally, common wheat (Triticum aestivum L.) provides approximately 20% of the calories and proteins consumed in the human diet [1] and in the United States, ranks third among field crops in planted acreage, production, and gross farm receipts [2]. Among arthropod pests and phytopathogens that reduce wheat yields, one of the most important is the wheat curl mite, (WCM), Aceria tosichella Keifer (Acari: Eriophyidae) which affects wheat production in the Americas, Australia, Europe, and Asia [reviewed in Refs. [3,4,5••]. Eriophyid mites are microscopic arthropods about 0.2 mm in length that usually infest young wheat leaves causing them to curl, hence the name wheat curl mite (Figure 1a). The mite causes direct physical damage by feeding, which can cause mild yield reductions [6]. More importantly, the WCM is the sole vector of four viruses, Wheat streak mosaic virus (family Potyviridae/genus Tritimovirus; WSMV) [7], Triticum mosaic virus (Potyviridae/Poacevirus; TriMV) [8], High Plains wheat mosaic virus (Fimoviridae/Emaravirus; HPWMoV) [9], and Brome streak mosaic virus (Potyviridae/Tritimovirus; BrSMV) [10]. Because of their common transmission and the difficulty in distinguishing symptoms, these diseases are commonly known as the wheat streak mosaic (WSM) complex. Of these viruses, WSMV is considered to have the greatest economic impact worldwide¸ whereas BrSMV is only found in Europe and does not cause economic losses [11,12]. Plants infected with WSMV show yellow to light green streaks that coalesce to form a mosaic pattern (Figure 1b). Symptoms are more severe if plants are infected early in their development and can include stunting, poor fertility/sterility, and reduced grain set [reviewed in Refs. 3,13]. Although single infections of WSMV occur more frequently compared to TriMV and HPWMoV, co-infections by two or all three viruses are common, which can exacerbate yield losses [14]. Average yield losses range from 2 to 3%, but localized affected areas can have much more dramatic losses of up to 100% [15]. In Kansas, the statewide five-year average yield loss to the wheat crop is 1.74%, but in 2017, reached 5.6%, resulting in $76.8 million lost revenue for Kansas wheat farmers [16].

The management of WCM and the disease complex has focused on an Integrated Pest Management (IPM) approach that combines host plant resistance to both mite and viruses with cultural practices such as controlling oversummering alternate hosts such as volunteer wheat, corn and wild grassy weeds [17]. These hosts serve as a ‘green bridge’ refuge for WCMs between harvesting of the mature wheat and the newly emerging winter wheat in fall. However, mites can infest over 90 other grass species and can travel distances of up to 3.3 km in wind currents during a single fall season [18], meaning that the effective control of secondary hosts is often impractical [11]. Delayed planting can also reduce fall infections by minimizing the overlap between the wheat crop and secondary hosts [19]. However, due to limited soil moisture in dryland production systems and time constraints associated with increasing farm size, it is often impractical to delay planting. Chemical control strategies are ineffective because WCM occupies secluded areas on the plant such as leaf sheaths and rolled and curled leaves [11] and there are no cost-effective miticides for use in wheat [20]. Moreover, there is accumulating evidence for apparent adaptation of mites to resistance genes [21,22] and novel resistance-breaking virus isolates [23,24,25]. Hence, there is an urgent need for alternative and effective control strategies for this complex pathosystem. In this review, we will highlight recent progress and future challenges for understanding host resistance to mites and viruses, with a focus on genetic diversity and its implications.

Section snippets

Host plant resistance to WSMV and WCM

Because of the difficulties of WCM management, developing crop varieties carrying genetic factors that either confer virus resistance and/or reduce WCM reproductive success are likely to be the most effective strategies to reduce yield losses from this disease complex. However, only two significant loci for WSMV resistance were detected in a winter wheat association mapping panel [26], highlighting the limited number of resistance loci in common wheat cultivars. Currently, there are just four

Genetic diversity and its implications

The effectiveness of host genetic resistance also varies according to genetic diversity in both WCMs and the viruses. There is great genetic variation among WCM populations including cryptic diversity (i.e., morphologically similar but genetically different individuals) as determined by analysis of mtDNA and nuclear markers [50]. For instance, Skoracka et al. [51] identified at least 16 different genotypes with numerous host associations and specificity in Poland. In North America, only two

Future research directions

A priority for future research will be to characterize Cmc and Wsm resistance genes, providing opportunities to identify and engineer novel resistance alleles acting in the same genetic and metabolic pathways. The identification of these genes will be invaluable for researchers to understand the mechanisms by which Cmc alleles impact WCM behavior and reproduction, and how Wsm alleles reduce viral replication. This knowledge will also help us evaluate the impact of genetic variation in WCM

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

This work was partially funded by the Colorado Wheat Research Foundation and Colorado Wheat Administrative Committee. We thank Marion Harris and Andy Michel for the invitation to contribute this manuscript.

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