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Temporally coordinated expression of nuclear genes encoding chloroplast proteins in wheat promotes Puccinia striiformis f. sp. tritici infection.

ABSTRACT: Targeting host processes that allow pathogens to thrive can be invaluable in resistance breeding. Here, we generated a deep-sequencing transcriptome time course for Puccinia striiformis f. sp. tritici (Pst) infection on wheat and compared datasets from three wheat varieties with different levels of susceptibility to two tested pathogen isolates. We sought genes specifically altered in a susceptible host as candidates that might support colonisation. Host responses differed between Pst-varietal pairs most prominently early during infection. Notably, however, nuclear genes encoding chloroplast-localised proteins (NGCPs) exhibited temporal coordination of expression profiles that differed at later time points in relation to Pst susceptibility. Disrupting one such NGCP, encoding the chloroplast-localised RNA binding protein TaCSP41a, led to lower Pst susceptibility. These analyses thus highlight NGCPs as prime targets for Pst manipulation during infection and point to TaCSP41a disruption as a potential source of Pst resistance for breeding programmes.

SUBMITTER: Corredor-Moreno P

PROVIDER: S-EPMC9395331 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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Temporally coordinated expression of nuclear genes encoding chloroplast proteins in wheat promotes Puccinia striiformis f. sp. tritici infection.

Corredor-Moreno Pilar P Badgami Roshani R Jones Sally S Saunders Diane G O DGO

Communications biology 20220822 1

Targeting host processes that allow pathogens to thrive can be invaluable in resistance breeding. Here, we generated a deep-sequencing transcriptome time course for Puccinia striiformis f. sp. tritici (Pst) infection on wheat and compared datasets from three wheat varieties with different levels of susceptibility to two tested pathogen isolates. We sought genes specifically altered in a susceptible host as candidates that might support colonisation. Host responses differed between Pst-varietal p ...[more]

PMID: 35996019

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Project description:Stripe rust [caused by Puccinia striiformis Westend. f. sp. tritici Eriks. (Pst)] is a destructive disease of wheat (Triticum aestivum L.) worldwide. Genetic resistance is the preferred method for control and the Yr5 gene, originally identified in Triticum spelta var. album, represents a major resistance (R) gene that confers all-stage resistance to all currently known races of Pst in the United States. To identify transcripts associated with the Yr5-mediated incompatible interaction and the yr5-compatible interaction, the Wheat GeneChip was used to profile the changes occurring in wheat isolines that differed for the presence of the Yr5 gene after inoculation with Pst. This time-course study (6, 12, 24 and 48 h post-inoculation) identified 115 transcripts that were induced during the R-gene-mediated incompatible interaction, and 73 induced during the compatible interaction. Fifty-four transcripts were induced in both interactions and were considered as basal defence transcripts, whilst 61 transcripts were specific to the incompatible interaction [hypersensitive response (HR)-specific transcripts] and 19 were specific to the compatible interaction (biotrophic interaction-specific transcripts). The temporal pattern of transcript accumulation showed a peak at 24 h after infection that may reflect haustorial penetration by Pst at ~16 h. An additional 12 constitutive transcript differences were attributed to the presence of Yr5 after eliminating those considered as incomplete isogenicity. Annotation of the induced transcripts revealed that the presence of Yr5 resulted in a rapid and amplified resistance response involving signalling pathways and defence-related transcripts known to occur during R-gene-mediated responses, including protein kinase signalling and the production of reactive oxygen species leading to a hypersensitive response. Basal defence also involved substantial induction of many defence-related transcripts but the lack of R-gene signalling resulted in weaker response.

Project description:The stripe rust of wheat is one of the devastating diseases in China, which is caused by fungus Puccinia striiformis f. sp. tritici (Pst). The Yunnan Province of China is located in the south-western part, and holds distinctive geographical and climate features, while wheat growth and epidemics of stripe rust fungus are fully dissimilar to the major wheat-growing regions of China. It is important to discover its origin and migration to control the disease. In this study, 352 isolates were sampled from 11 spots of the Yunnan Province during the wheat growing season from 2004 to 2015 and analyzed with SNPs markers of housekeeping genes. Results revealed that 220 haplotypes were inferred from the concatenating sequences; among them, 5 haplotypes (viz., 'H86', 'H18', 'H8', 'H15' and 'H23') comprised over 24.5% of the population. The haplotype diversity, nucleotide diversity, mutation rate and recombination events were 0.992, 6.04 × 10-3, 4.46 × 10-3 and 18.0 respectively, which revealed the genetic diversity of Pst populations among all locations. Four grouping methods, such as UPGMA-tree, PCA, PLS-DA and STRUCTURE, were employed for the categorization of the Pst populations conferring to their races and topographical localities. All methods were found significant and mostly had co-linear relations with each other. The analysis of molecular variance (AMOVA) conferred total variation was 9.09%, and 86.20% of variation was within the populations. The current study also exposed a comparatively high genetic multiplicity within the population, while low genetic inconsistency among the populations. Furthermore, the molecular records on the gene pole (Nm = 18.45) established that the migration of the stripe rust pathogen occurred among all locations in Yunnan province. The ancestral haplotype was detected in Yuxi. Based on the trajectories of upper airflow and genetic diversity of Pst populations in different locations, it is suggested that the locations Dehong, Dali, Lincang and Baoshan are probably a major source of Pst in Yunnan.

Dataset Information

Temporally coordinated expression of nuclear genes encoding chloroplast proteins in wheat promotes Puccinia striiformis f. sp. tritici infection.

Publications

Temporally coordinated expression of nuclear genes encoding chloroplast proteins in wheat promotes Puccinia striiformis f. sp. tritici infection.

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