Gene Structure-Based Homology Search Identifies Highly Divergent Putative Effector Gene Family

Abstract

Homology of highly divergent genes often cannot be determined from sequence similarity alone. For example, we recently identified in the aphid Hormaphis cornu a family of rapidly evolving bicycle genes, which encode novel proteins implicated as plant gall effectors, and sequence similarity search methods yielded few putative bicycle homologs in other species. Coding sequence-independent features of genes, such as intron-exon boundaries, often evolve more slowly than coding sequences, however, and can provide complementary evidence for homology. We found that a linear logistic regression classifier using only structural features of bicycle genes identified many putative bicycle homologs in other species. Independent evidence from sequence features and intron locations supported homology assignments. To test the potential roles of bicycle genes in other aphids, we sequenced the genome of a second gall-forming aphid, Tetraneura nigriabdominalis, and found that many bicycle genes are strongly expressed in the salivary glands of the gall forming foundress. In addition, bicycle genes are strongly overexpressed in the salivary glands of a non-gall forming aphid, Acyrthosiphon pisum, and in the non-gall forming generations of Hormaphis cornu. These observations suggest that Bicycle proteins may be used by multiple aphid species to manipulate plants in diverse ways. Incorporation of gene structural features into sequence search algorithms may aid identification of deeply divergent homologs, especially of rapidly evolving genes involved in host-parasite interactions.

Tertiary structure assessment at CASP15

“…They are both small (159 and 172 residues, respectively), largely α‐helical, monomeric, and were singletons in the main sequence databases at the time of CASP. A handful of good quality models of T1130 were submitted by groups who apparently discovered additional homologous sequences in the Supporting Information of a paper 51 or in databases not searched by other groups.…”

Alternative splicing regulation in plants by effectors of symbiotic arbuscular mycorrhizal fungi

“…The exon-intron structure has been used to identify a common origin for other effectors, including the Y/F/WxC effector family from the pathogenic fungus Blumeria graminis f.sp. hordei 47 or the Bicycle effectors from aphids 48 . Using the criteria of this conserved signature and the conserved intron, we found that SP7-like proteins are present in the Glomerales and Diversisporales, but there are so far no hints of them in more ancient orders such as Paraglomerales or Archaeosporales nor in other subphyla from the Mucoromycota such as Morteriellomycotina or Mucoromycotina (Fig.…”

Molecular Aspects of Gall Formation Induced by Mites and Insects

“…The molecular mechanisms underlying these processes are still unclear. The latest advances in this field involved the detection of the active expression of several secreted proteins (potential effectors) in the salivary glands of gall-forming aphids [ 51 , 52 ], as well as in the ovaries and venom glands of galling wasps [ 40 ].…”

“…Bicycle genes are strongly expressed in the aphid’s salivary glands [ 51 ]. The same group of researchers later discovered that many bicycle genes are strongly expressed not only in the salivary glands of a second galling aphid, Tetraneura nigriabdominalis (Sasaki, 1899), but also in the salivary glands of a non-gall forming aphid, Acyrthosiphon pisum (Harris, 1776), as well as in the non-gall forming generation of Hormaphis cornu [ 52 ]. Those researchers hypothesized that “these observations suggest that BICYCLEproteins may be used by multiple aphid species to manipulate plants in diverse ways” [ 52 ]: (p. 1).…”