Sequence diversification in recessive alleles of two host factor genes suggests adaptive selection for bymovirus resistance in cultivated barley from East Asia

Abstract

Key message Two distinct patterns of sequence diversity for the recessive alleles of two host factors HvPDIL5 - 1 and HvEIF4E indicated the adaptive selection for bymovirus resistance in cultivated barley from East Asia. AbstractPlant pathogens are constantly challenging plant fitness and driving resistance gene evolution in host species. Little is known about the evolution of sequence diversity in host recessive resistance genes that interact with plant viruses. Here, by combining previously published and newly generated targeted re-sequencing information, we systematically analyzed natural variation in a broad collection of wild (Hordeum spontaneum; Hs) and domesticated barleys (Hordeum vulgare; Hv) using the full-length coding sequence of the two host factor genes, HvPDIL5-1 and HvEIF4E, conferring recessive resistance to the agriculturally important Barley yellow mosaic virus (BaYMV) and Barley mild mosaic virus (BaMMV). Interestingly, two types of gene evolution conferred by sequence variation in domesticated barley, but not in wild barley were observed. Whereas resistance-conferring alleles of HvEIF4E exclusively contained non-synonymous amino acid substitutions (including in-frame sequence deletions and insertions), loss-of-function alleles were predominantly responsible for the HvPDIL5-1 conferred bymovirus resistance. A strong correlation between the geographic origin and the frequency of barley accessions carrying resistance-conferring alleles was evident for each of the two host factor genes, indicating adaptive selection for bymovirus resistance in cultivated barley from East Asia.Electronic supplementary materialThe online version of this article (doi:10.1007/s00122-016-2814-z) contains supplementary material, which is available to authorized users.

Good Riddance? Breaking Disease Susceptibility in the Era of New Breeding Technologies

“…Naturally occurring variation of S genes can be identified by EcoTILLING: re-sequencing S genes in natural populations of crop progenitors or land races. EcoTILLING identified a new allele of eIF4E for melon necrotic spot virus resistance [85], and similar to our previous example of HvPDIL5-1, a TILLING approach further confirmed the identity of the mutated S gene in rym1 genotypes [83]. Figure 2.…”

“…In barley, the viral S factor HvEIF4E also occurs in many diverse resistance-conferring haplotypes. For another unrelated virus S gene, HvPDIL5-1, many haplotypes are present in wild barley and landraces, yet none of these are actual virus resistance conferring alleles (rym-alleles) [82,83]. The fact that several barley cultivars with different resistance conferring alleles exist, does suggest that the s alleles arose by mutation during domestication in an area where the virus was also present [83].…”

“…For another unrelated virus S gene, HvPDIL5-1, many haplotypes are present in wild barley and landraces, yet none of these are actual virus resistance conferring alleles (rym-alleles) [82,83]. The fact that several barley cultivars with different resistance conferring alleles exist, does suggest that the s alleles arose by mutation during domestication in an area where the virus was also present [83]. Also, Tsn1 shows large variety in spelt and other grasses, but in turn, it has hardly any polymorphisms in bread and durum wheat [9].…”

High-resolution mapping ofRym14Hb, a wild relative resistance gene to barley yellow mosaic disease

“…To date, 20 barley resistance genes have been identified, almost exclusively conferring recessive resistance (Jiang et al 2020). Two of these loci have been cloned: the EUKARYOTIC TRANSLATION INITIATION FACTOR 4E gene (eIF4E), (Stein et al 2005) of which several allelic forms providing resistance are described, including rym4 and rym5, (Hofinger et al 2011;Perovic et al 2014;Yang et al 2017;Shi et al 2019), and the PROTEIN DISULFIDE ISOMERASE LIKE 5-1 (PDI5-1) gene which is also represented by a handful of alleles providing resistance, including rym1 and rym11 (Yang et al 2017). The rym4 allele provides resistance to BaMMV and to the common BaYMV pathotype BaYMV-1, but not to pathotype BaYMV-2, which emerged in Europe at the end of the 1980s (Adams et al 1987;Huth 1989;Adams 1991;Graner and Bauer 1993;Steyer et al 1995).…”

Mimicking natural polymorphism in eIF4E by CRISPR‐Cas9 base editing is associated with resistance to potyviruses

“…By separately analysing each mutation from a natural resistance allele, we wanted to assess the role of each mutation in resistance and determine the minimal number of AA changes needed to achieve resistance in plants. Usually, the effect of AA changes can be assessed by the analysis of natural allelic series or by overexpression studies in a resistant background, as has been done for several studied pathosystems (Ashby et al ., ; Charron et al ., ; German‐Retana et al ., ; Yang et al ., ). Our conclusions were consistent with and confirm previous studies (Ashby et al ., ; German‐Retana et al ., ; Kim et al ., ), showing that most mutations selected among those found naturally do not affect the role of eIF4E factor in translation initiation.…”