ABSTRACT
Maize (Zea mays subsp. mays) yield loss from arthropod herbivory is substantial. While the basis of resistance to major insect herbivores has been comparatively well-studied in maize, less is known about resistance to spider mite herbivores, which are distantly related to insects and feed by a different mechanism. Two spider mites, the generalist Tetranychus urticae, and the grass-specialist Oligonychus pratensis, are notable pests of maize, especially during drought conditions. We assessed resistance (antibiosis) to both mites of 38 highly diverse maize lines, including several previously reported to be resistant to one or the other mite species. We found that line B96, as well as its derivatives B49 and B75, were highly resistant to T. urticae. In contrast, neither these three lines, nor any others included in our study, were notably resistant to the specialist O. pratensis. Quantitative trait locus (QTL) mapping with replicate populations from crosses of B49, B75, and B96 to susceptible B73 identified a QTL in the same genomic interval on chromosome 6 for T. urticae resistance in each of the three resistant lines, and an additional resistance QTL on chromosome 1 was unique to B96. Single-locus genotyping with a marker coincident with the chromosome 6 QTL in crosses of both B49 and B75 to B73 revealed that the respective QTL was large-effect; it explained â¼70% of the variance in resistance, and resistance alleles from B49 and B75 acted recessively as compared to B73. Finally, a genome-wide haplotype analysis using genome sequence data generated for B49, B75, and B96 identified an identical haplotype, likely of initial origin from B96, as the source of T. urticae resistance on chromosome 6 in each of the B49, B75, and B96 lines. Our findings uncover the relationship between intraspecific variation in maize defenses and resistance to its major generalist and specialist spider mite herbivores, and we identified loci for use in breeding programs and for genetic studies of resistance to T. urticae, the most widespread spider mite pest of maize.
ABSTRACT
While substantial progress has been made in understanding defense responses of cereals to insect herbivores, comparatively little is known about responses to feeding by spider mites. Nevertheless, several spider mite species, including the generalist Tetranychus urticae and the grass specialist Oligonychus pratensis, cause damage on cereals such as maize and wheat, especially during drought stress. To understand defense responses of cereals to spider mites, we characterized the transcriptomic responses of maize and barley to herbivory by both mite species, and included a wounding control against which modulation of defenses could be tested. T. urticae and O. pratensis induced highly correlated changes in gene expression on both maize and barley. Within 2 h, hundreds of genes were upregulated, and thousands of genes were up- or downregulated after 24 h. In general, expression changes were similar to those induced by wounding, including for genes associated with jasmonic acid biosynthesis and signaling. Many genes encoding proteins involved in direct defenses, or those required for herbivore-induced plant volatiles, were strongly upregulated in response to mite herbivory. Further, biosynthesis genes for benzoxazinoids, which are specialized compounds of Poaceae with known roles in deterring insect herbivores, were induced in maize. Compared to chewing insects, spider mites are cell content feeders and cause grossly different patterns of tissue damage. Nonetheless, the gene expression responses of maize to both mite herbivores, including for phytohormone signaling pathways and for the synthesis of the benzoxazinoid 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside, a known defensive metabolite against caterpillars, resembled those reported for a generalist chewing insect, Spodoptera exigua. On maize plants harboring mutations in several benzoxazinoid biosynthesis genes, T. urticae performance dramatically increased compared to wild-type plants. In contrast, no difference in performance was observed between mutant and wild-type plants for the specialist O. pratensis. Collectively, our data provide little evidence that maize and barley defense responses differentiate herbivory between T. urticae and O. pratensis. Further, our work suggests that the likely route to specialization for O. pratensis involved the evolution of a robust mechanism to cope with the benzoxazinoid defenses of its cereal hosts.
