Abstract

Potatoes are the world’s most produced non-grain crops and an important food source for billions of people. Potatoes are susceptible to numerous pathogens that reduce yield, including Potato virus Y (PVY). Genetic resistance to PVY is a sustainable way to limit yield and quality losses due to PVY infection. Potato cultivars vary in their susceptibility to PVY and include susceptible varieties such as Russet Burbank, and resistant varieties such as Payette Russet. Although the loci and genes associated with PVY-resistance have been identified, the genes and mechanisms involved in limiting PVY during the development of systemic infections have yet to be fully elucidated. To increase our understanding of PVY infection, potato antiviral responses, and resistance, we utilized RNA sequencing to characterize the transcriptomes of two potato cultivars. Since transcriptional responses associated with the extreme resistance response occur soon after PVY contact, we analyzed the transcriptome and small RNA profile of both the PVY-resistant Payette Russet cultivar and PVY-susceptible Russet Burbank cultivar 24 hours post-inoculation. While hundreds of genes, including terpene synthase and protein kinase encoding genes, exhibited increased expression, the majority, including numerous genes involved in plant pathogen interactions, were downregulated. To gain greater understanding of the transcriptional changes that occur during the development of systemic PVY-infection, we analyzed Russet Burbank leaf samples one week and four weeks post-inoculation and identified similarities and differences, including higher expression of genes involved in chloroplast function, photosynthesis, and secondary metabolite production, and lower expression of defense response genes at those time points. Small RNA sequencing identified different populations of 21- and 24-nucleotide RNAs and revealed that the miRNA profiles in PVY-infected Russet Burbank plants were similar to those observed in other PVY-tolerant cultivars and that during systemic infection ~32% of the NLR-type disease resistance genes were targeted by 21-nt small RNAs. Analysis of alternative splicing in PVY-infected potato plants identified splice variants of several hundred genes, including isoforms that were more dominant in PVY-infected plants. The description of the PVYN-Wi-associated transcriptome and small RNA profiles of two potato cultivars described herein adds to the body of knowledge regarding differential outcomes of infection for specific PVY strain and host cultivar pairs, which will help further understanding of the mechanisms governing genetic resistance and/or virus-limiting responses in potato plants.

Highlights

  • Potato (Solanum tuberosum) is the third most important food crop, in terms of worldwide production, with nearly 400 million metric tons produced per year [1]

  • To characterize the transcriptional responses of Potato virus Y (PVY)-susceptible Russet Burbank plants during development of systemic infection, plants were sampled at three time points after infection (24 hpi, 1 wpi, and 4 wpi) with the inoculated leaf being sampled at 24 hpi, and upper, uninoculated leaves sampled at the later time points

  • To gain a better understanding of potato antiviral responses, we examined the transcript and small RNA profiles of PVY strain Wilga (PVYN-Wi) -infected Russet Burbank plants at three time points post-infection which included the development of systemic infection, and in one matching early time point post-inoculation (i.e., 24 hpi) in Payette Russet, a cultivar that exhibits extreme PVY-resistance

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Summary

Introduction

Potato (Solanum tuberosum) is the third most important food crop, in terms of worldwide production, with nearly 400 million metric tons produced per year [1]. The global human population is projected to grow by two billion by the year 2050 with the most growth occurring in developing countries [2]. Planting crops that are more resistant to pathogens and abiotic stressors and, require fewer inputs is one way to minimize the impact of agriculture. Potatoes are reliably grown in diverse landscapes and environmental conditions, but abiotic and biotic stressors, including water stress, heat stress, and pathogens can negatively impact yield and tuber quality [3]. Reliance upon clonal propagation renders potato production more vulnerable to vertical pathogen transmission and spread as compared to crops planted with true seed [4]

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