Mechanisms of nuclear suppression of host immunity by effectors from the Arabidopsis downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa).

Filamentous phytopathogens form sophisticated intracellular feeding structures called haustoria in plant cells. Pathogen effectors are likely to play a role in the establishment and maintenance of haustoria additional to their more characterized role of suppressing plant defense. Recent studies suggest that effectors may manipulate host transcription or other nuclear regulatory components for the benefit of pathogen development. However, the specific mechanisms by which these effectors promote susceptibility remain unclear. Of two recent screenings, we identified 15 nuclear-localized Hpa effectors (HaRxLs) that interact directly or indirectly with host nuclear components. When stably expressed in planta, nuclear HaRxLs cause diverse developmental phenotypes highlighting that nuclear effectors might interfere with fundamental plant regulatory mechanisms. Here, we report recent advances in understanding how a pathogen can manipulate nuclear processes in order to cause disease.

Quantitative genetics of feeding behavior in two ecological races of the pea aphid, Acyrthosiphon pisum.

Much of the diversity of herbivorous insects stems from the adaptive divergence of populations onto different host plants. This often involves the evolution of specialized patterns of host acceptance that in turn lead to assortative mating for insects that mate exclusively on their hosts. Here, we explore the genetic architecture of feeding behavior in a herbivorous insect that has become a model for the study of incipient speciation, the pea aphid (Acyrthosiphon pisum). We use crosses between individuals specialized to either alfalfa or red clover in order to perform both a biometrical analysis and a quantitative trait locus (QTL) analysis of key feeding behaviors. For each character in each environment, Castle-Wright's estimator for the number of effective factors segregating ranged from 0.11 to 2.54. Similarly, between 0 and 3 QTLs were detected. In one case, a single QTL explained over 50% of the variance in the F2, suggesting that at least one gene (or a complex of tightly linked genes) has a major effect on feeding behavior in the pea aphid. However, the identified QTL explain only 23-73% of the genetic variance for these characters thus additional genes of minor effect are also involved. We found a variety of modes of gene action, including several cases of non-additive gene action. Our results suggest that feeding behavior in pea aphids is neither simple nor highly polygenic. The oligogenetic basis of variation in feeding behavior may facilitate host shifts, providing one explanation for the frequent divergence and speciation of herbivorous insects.

Biometrical genetic analysis of luteovirus transmission in the aphid Schizaphis graminum.

The aphid Schizaphis graminum is an important vector of the viruses that cause barley yellow dwarf disease. We studied the genetic architecture of virus transmission by crossing a vector and a non-vector genotype of S. graminum. F1 and F2 hybrids were generated, and a modified line-cross biometrical analysis was performed on transmission phenotype of two of the viruses that cause barley yellow dwarf: Cereal yellow dwarf virus (CYDV)-RPV and Barley yellow dwarf virus (BYDV)-SGV. Our aims were to (1) determine to what extent differences in transmission ability between vectors and non-vectors is due to net additive or non-additive gene action, (2) estimate the number of loci that determine transmission ability and (3) examine the nature of genetic correlations between transmission of CYDV-RPV and BYDV-SGV. Only additive effects contributed significantly to divergence in transmission of both CYDV-RPV and BYDV-SGV. For each luteovirus, Castle-Wright's estimator for the number of effective factors segregating for transmission phenotype was less than one. Transmission of CYDV-RPV and BYDV-SGV was significantly correlated in the F2 generation, suggesting that there is a partial genetic overlap for transmission of these luteoviruses. Yet, 63% of the F2 genotypes transmitted CYDV-RPV and BYDV-SGV at significantly different rates. Our data suggest that in S. graminum, the transmission efficiency of both CYDV-RPV and BYDV-SGV is regulated by a major gene or set of tightly linked genes, and the transmission efficiency of each virus is influenced by a unique set of minor genes.

Genetic Regulation of Polerovirus and Luteovirus Transmission in the Aphid Schizaphis graminum.

ABSTRACT Sexual forms of two genotypes of the aphid Schizaphis graminum, one a vector, the other a nonvector of two viruses that cause barley yellow dwarf disease (Barley yellow dwarf virus [BYDV]-SGV, luteovirus and Cereal yellow dwarf virus-RPV, polerovirus), were mated to generate F1 and F2 populations. Segregation of the transmission phenotype for both viruses in the F1 and F2 populations indicated that the transmission phenotype is under genetic control and that the parents are heterozygous for genes involved in transmission. The ability to transmit both viruses was correlated within the F1 and F2 populations, suggesting that a major gene or linked genes regulate the transmission. However, individual hybrid genotypes differed significantly in their ability to transmit each virus, indicating that in addition to a major gene, minor genes can affect the transmission of each virus independently. Gut and salivary gland associated transmission barriers were identified in the nonvector parent and some progeny, while other progeny possessed only a gut barrier or a salivary gland barrier. Hemolymph factors do not appear to be involved in determining the transmission phenotype. These results provide direct evidence that aphid transmission of luteoviruses is genetically regulated in the insect and that the tissue-specific barriers to virus transmission are not genetically linked.

Genetic mapping of aphicarus -- a sex-linked locus controlling a wing polymorphism in the pea aphid (Acyrthosiphon pisum).

We have initiated research to determine the genetic basis of a male wing polymorphism in the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae). Previous studies showed that this polymorphism is controlled by a single biallelic locus, which we name aphicarus (api), on the X chromosome. Our objectives were to confirm that api segregates as a polymorphism of a single gene on the X chromosome, and to obtain molecular markers flanking api that can be used as a starting point for high-resolution genetic and physical mapping of the target region, which will ultimately allow the cloning of api. We have established an F2 population segregating for api and have generated X-linked AFLP markers. The segregation pattern of api in the F2 population shows that the male wing polymorphism segregates as a polymorphism of a single gene, or set of closely linked genes on the X chromosome. Using a subset of 78 F2 males, we have constructed a linkage map of the chromosomal region encompassing api using seven AFLP markers. The map spans 74.1 cM and we have mapped api to an interval of 10 cM. In addition, we confirmed X linkage of our AFLP markers and api by using one X-linked marker developed in an earlier study. Our study presents the first mapping of a gene with known function in aphids, and the results indicate that target gene mapping in aphids is feasible.

A sex-linked locus controls wing polymorphism in males of the pea aphid, Acyrthosiphon pisum (Harris).

Discrete variation in wing morphology is a very common phenomenon in insects and has been used extensively in the past 50 years as a model to study the ecology and evolution of dispersal. Wing morph determination can be purely genetic, purely environmental, or some combination of the two. The precise genetic determinants of genetically based wing morph variation are unknown. Here we explore the genetic basis of wing polymorphism in the pea aphid, which can produce either winged or wingless males. We confirm that three types of pea aphid clones coexist in natural populations, those producing winged males only, those producing wingless males only, and those producing a mixture of both. A Mendelian genetic analysis reveals that male wing polymorphism in pea aphids is determined by a single locus, two alleles system. Using microsatellite loci of known location, we show that this locus is on the X chromosome. The existence of a simple genetic determinism for wing polymorphism in a system in which genetic investigation is possible may help investigations on the physiological and molecular mechanisms of genetically-based wing morph variation. This locus could also be used in the search for genes involved in the wing polyphenism described in parthenogenetic females and to investigate the interplay between polymorphisms and polyphenisms.