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Virulence adaptation in a rice leafhopper: Exposure to ineffective genes compromises pyramided resistance.

ABSTRACT: Pyramiding resistance genes is predicted to increase the durability of resistant rice varieties against phloem-feeding herbivores. We examined responses by the green leafhopper, Nephotettix virescens (Hemiptera: Cicadellidae), to near-isogenic rice lines with zero, one and two resistance genes. The recurrent parent (T65) and monogenic lines (GRH2-NIL and GRH4-NIL) with genes for resistance to the green rice leafhopper, Nephotettix cincticeps (Hemiptera: Cicadellidae), were susceptible to the green leafhopper, but the pyramided line (GRH2/GRH4-PYL) was highly resistant to the green leafhopper. We selected green leafhoppers, N. virescens, from five sites in the Philippines for over 20 generations on each of the four lines. Populations selected on GRH2/GRH4-PYL gained partial virulence (feeding and development equal to that on T65) to the pyramided line within 10 generations and complete virulence (egg-laying equal to that on T65) within 20 generations. After 20 generations of rearing on the susceptible monogenic lines, green leafhoppers were also capable of developing and laying eggs on GRH2/GRH4-PYL. Furthermore, green leafhoppers reared on the susceptible GRH4-NIL for 20 generations showed equal preferences for T65 and GRH2/GRH4-PYL in choice bioassays. Our results indicate that previous long-term exposure to ineffective genes (including unperceived resistance genes) could dramatically reduce the durability of pyramided resistance. We suggest that informed crop management and deployment strategies should be developed to accompany rice lines with pyramided resistance and avoid the build-up of virulent herbivore populations.

SUBMITTER: Horgan FG

PROVIDER: S-EPMC6106693 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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Virulence adaptation in a rice leafhopper: Exposure to ineffective genes compromises pyramided resistance.

Horgan Finbarr G FG Bernal Carmencita C CC Vu Quynh Q Almazan Maria Liberty P MLP Ramal Angelee Fame AF Yasui Hideshi H Fujita Daisuke D

Crop Protection. 20181101

Pyramiding resistance genes is predicted to increase the durability of resistant rice varieties against phloem-feeding herbivores. We examined responses by the green leafhopper, Nephotettix virescens (Hemiptera: Cicadellidae), to near-isogenic rice lines with zero, one and two resistance genes. The recurrent parent (T65) and monogenic lines (GRH2-NIL and GRH4-NIL) with genes for resistance to the green rice leafhopper, Nephotettix cincticeps (Hemiptera: Cicadellidae), ...[more]

PMID: 30393420

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Project description:BackgroundEmergence of new pathogen strains of Magnaporthe oryzae is a major reason for recurrent failure of the resistance mediated by a single resistance gene (Pi) in rice. Stacking various Pi genes in the genome through marker-assisted selection is thus an effective strategy in rice breeding for achieving durable resistance against the pathogen. However, the effect of pyramiding of multiple Pi genes using transgenesis still remains largely unknown.ResultsThree Pi genes Pib, Pi25 and Pi54 were transferred together into two rice varieties, the indica variety Kasalath and the japonica variety Zhenghan 10. Transgenic plants of both Kasalath and Zhenghan 10 expressing the Pi transgenes showed imparted pathogen resistance. All the transgenic lines of both cultivars also exhibited shorter growth periods with flowering 2-4 days early, and shorter plant heights with smaller panicle. Thus, pyramiding of the Pi genes resulted in reduced grain yields in both rice cultivars. However, tiller numbers and grain weight were generally similar between the pyramided lines and corresponding parents. A global analysis of gene expression by RNA-Seq suggested that both enhancement and, to a lesser extent, inhibition of gene transcription occurred in the pyramided plants. A total of 264 and 544 differentially expressed genes (DEGs) were identified in Kasalath and Zhenghan 10, respectively. Analysis of the DEGs suggested that presence of the Pi transgenes did not alter gene expression only related to disease resistance, but also impacted many gene transcriptions in the pathways for plant growth and development, in which several were common for both Kasalath and Zhenghan 10.ConclusionPyramiding of the Pi genes Pib, Pi25 and Pi54 via transgenesis is a potentially promising approach for improving rice resistance to the pathogen Magnaporthe oryzae. However, pleiotropic effects of the Pi genes could potentially result in yield loss. These findings support the idea that immunity is often associated with yield penalties. Rational combination of the Pi genes based on the genetic background may be important to balance yield and disease resistance.

Project description:Background and aimsMicroRNAs (miRNAs) are small non-coding RNAs that act as post-transcriptional regulators of gene expression via sequence-specific cleavage or translational repression of target transcripts. They are transcribed as long single-stranded RNA precursors with unique stem-loop structures that are processed by a DICER-Like (DCL) ribonuclease, typically DCL1, to produce mature miRNAs. Although a plethora of miRNAs have been found to be regulated by pathogen infection in plants, the biological function of most miRNAs remains largely unknown. Here, the contribution of OsDCL1 to rice immunity was investigated.MethodsActivation-tagged Osdcl1a (Osdcl1a-Ac) rice mutants were examined for resistance to pathogen infection. mRNA and small RNA deep sequencing, quantitative real-time PCR (RT-qPCR) and stem-loop reverse tanscripion-PCR (RT-PCR) were used to examine DCL1a-mediated alterations in the rice transcriptome. Rice diterpene phytoalexins were quantified by liquid chromatography-tandem mass spectrometry (LC-MSMS). Accumulation of O2·- was determined by nitroblue tetrazolium (NBT) staining.Key resultsdcl1a-Ac mutants exhibit enhanced susceptibility to infection by fungal pathogens which was associated with a weaker induction of defence gene expression. Comparison of the mRNA and miRNA transcriptomes of dcl1a-Ac and wild-type plants revealed misregulation of genes involved in detoxification of reactive oxygen species. Consequently, dcl1a-Ac plants accumulated O2·- in their leaves and were more sensitive to methyl viologen-induced oxidative stress. Furthermore, dcl1a-Ac plants showed downregulation of diterpenoid phytoalexin biosynthetic genes, these genes also being weakly induced during pathogen infection. Upon pathogen challenge, dcl1a-Ac plants failed to accumulate major diterpenoid phytoalexins. OsDCL1a activation resulted in marked alterations in the rice miRNAome, including both upregulation and downregulation of miRNAs.ConclusionsOsDCL1a activation enhances susceptibility to infection by fungal pathogens in rice. Activation of OsDCL1a represses the pathogen-inducible host defence response and negatively regulates diterpenoid phytoalexin production. These findings provide a basis to understand the molecular mechanisms through which OsDCL1a mediates rice immunity.

Project description:We tested the hypotheses that increasing the number of anti-herbivore resistance loci in crop plants will increase resistance strength, increase the spectrum of resistance (the number of species affected), and increase resistance stability. We further examined the potential ecological costs of pyramiding resistance under benign environments. In our experiments, we used 14 near-isogenic rice lines with zero (T65: recurrent parent), one, two or three resistance loci introgressed through marker-assisted selection. Lines with two or more loci that were originally bred for resistance to the green rice leafhopper, Nephotettix cincticeps, significantly reduced egg-laying by the green leafhopper, N. virescens. Declines in egg-number and in nymph weight were correlated with the numbers of resistance loci in the rice lines. To test the spectrum of resistance, we challenged the lines with a range of phloem feeders including the zig-zag leafhopper, Recilia dorsalis, brown planthopper, Nilaparvata lugens, and whitebacked planthopper, Sogatella furcifera. There was an increase in the number of tested species showing significant declines in egg-laying and nymph survival on lines with increasing numbers of loci. In a screen house trial that varied rates of nitrogenous fertilizer, a line with three loci had stable resistance against the green leafhopper and the grain yields of infested plants were maintained or increased (overcompensation). Under benign conditions, plant growth and grain yields declined with increasing numbers of resistance loci. However, under field conditions with natural exposure to herbivores, there were no significant differences in final yields. Our results clearly indicate the benefits, including unanticipated benefits such as providing resistance against multiple herbivore species, of pyramiding anti-herbivore resistance genes/loci in crop plants. We discuss our results as part of a review of existing research on pyramided resistance against leafhoppers and planthoppers in rice. We suggest that potential ecological costs may be overcome by the careful selection of gene combinations for pyramiding, avoidance of high (potentially redundant) loci numbers, and introgression of loci into robust plant types such as hybrid rice varieties.

Project description:A new rice viral disease exhibiting distinct symptoms-yellow stripes, mosaic and twisted tips on leaves-was found in China. Electron microscopy of infected leaf cells revealed the presence of bacilliform virions and electron-translucent granular-fibrillar viroplasm in the cytoplasm. The enveloped viral particles were 300 to 375 nm long and 45 to 55 nm wide. The leafhopper Recilia dorsalis was able to transmit the virus to rice seedlings, which subsequently exhibited symptoms similar to those observed in fields. The complete genome of the virus was obtained by small-RNA deep sequencing and reverse transcription-PCR product sequencing. The anti-genome contains seven open reading frames (ORFs). The deduced amino acids of ORF1, ORF5, and ORF7 are, respectively, homologous to the nucleocapsid protein (N), glycoprotein (G), and large polymerase protein (L) of known rhabdoviruses. The predicted product of ORF2 is identified as a phosphoprotein (P) based on its multiple potential phosphorylation sites and 12.6 to 21.0% amino acid (aa) identities with the P proteins of plant rhabdoviruses. The product of ORF4 is presumed to be the viral matrix (M) protein for it shares 10.3 to 14.3% aa identities with those of other rhabdoviruses. The above five products were confirmed as the viral structural proteins by SDS-PAGE and aa sequencing analyses of purified virus preparation. ORF3 and ORF6 are considered to encode two nonstructural proteins with unknown functions. Phylogenetic analysis based on protein N, G, and L amino acid sequences indicated that the isolated virus, which we have tentatively named Rice stripe mosaic virus (RSMV), is a new species in the genus Cytorhabdovirus. To our knowledge, RSMV is the only cytorhabdovirus naturally infecting rice and the first reported leafhopper-transmitted cytorhabdovirus. Our surveys of rice fields indicate that RSMV occurs frequently in Guangdong Province, China. Although the disease incidence is low at present, it might become serious with the vector insect population increasing.

Dataset Information

Virulence adaptation in a rice leafhopper: Exposure to ineffective genes compromises pyramided resistance.

Publications

Virulence adaptation in a rice leafhopper: Exposure to ineffective genes compromises pyramided resistance.

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