Dual transcriptional characterization of spinach and Peronospora effusa during resistant and susceptible race-cultivar interactions

Authors: CLARK, KELLEY - University Of California; Feng, Chunda; Anchieta, Amy; VAN DEYNZE, ALLEN - University Of California; CORRELL, JAMES - University Of Arkansas; Klosterman, Steven

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/17/2024
Publication Date: 10/7/2024
Citation: Clark, K.J., Feng, C., Anchieta, A.G., Van Deynze, A., Correll, J.C., Klosterman, S.J. 2024. Dual transcriptional characterization of spinach and Peronospora effusa during resistant and susceptible race-cultivar interactions. BMC Genomics. 25. Article 937. https://doi.org/10.1186/s12864-024-10809-x.
DOI: https://doi.org/10.1186/s12864-024-10809-x

Interpretive Summary: Spinach is a popular and nutritious crop belonging to the plant family which also contains beet, chard, and quinoa. One of the major disease concerns for spinach remains Peronospora effusa which causes downy mildew. Spinach downy mildew renders crops unmarketable due to leaf chlorosis and masses of downy mildew spores which appear on the underside of leaves. There have been recent advances in the genomes of both spinach and P. effusa providing improved resources for analyzing gene expression in both the pathogen and the plant. This research describes gene expression profiles for spinach and P. effusa during resistant and susceptible interactions to different isolates of P. effusa. Further, the work maps some of the resistance type homolog genes from spinach to the different spinach chromosomes. This resource is valuable for breeding spinach with downy mildew disease resistance and valuable in ascertaining the mechanisms by which P. effusa invades spinach.

Technical Abstract: Spinach downy mildew, caused by the obligate oomycete pathogen, Peronospora effusa remains a major concern for spinach production. Disease control is predominantly based on development of resistant spinach cultivars. However, new races and novel isolates of the pathogen continue to emerge and overcome cultivar resistance. Currently there are 20 known races of P. effusa. Here we characterized the transcriptomes of spinach, Spinacia oleracea, and P. effusa during disease progression using the spinach cultivar Viroflay, the near isogenic lines NIL1 and NIL3, and P. effusa races, R13 and R19, at 24 h post inoculation and 6 days post inoculation. A total of 54 samples were collected and subjected to sequencing and transcriptomic analysis. Differentially expressed gene (DEG) analysis in resistant spinach interactions of R13-NIL1 and R19-NIL3 revealed spinach DEGs from protein kinase-like and P-loop containing families, which have roles in plant defense. The homologous plant defense genes included but were not limited to, receptor-like protein kinases (Spiol0281C06495, Spiol06Chr21559 and Spiol06Chr24027), a BAK1 homolog (Spiol0223C05961), genes with leucine rich repeat motifs (Spiol04Chr08771, Spiol04Chr01972, Spiol05Chr26812, Spiol04Chr11049, Spiol0084S08137, Spiol03Chr20299) and ABC-transporters (Spiol02Chr28975, Spiol06Chr22112, Spiol06Chr03998 and Spiol04Chr09723). Additionally, analysis of the expression of eight homologous to previously reported downy mildew resistance genes revealed that some are differentially expressed during resistant reactions but not during susceptible reactions. Examination of P. effusa gene expression during infection of susceptible cultivars identified expressed genes present in R19 or R13 including predicted RxLR and Crinkler effector genes that may be responsible for race-specific virulence on NIL1 or NIL3 spinach hosts, respectively. These findings deliver foundational insight to gene expression in both spinach and P. effusa during susceptible and resistant interactions and provide a library of candidate genes for further exploration and functional analysis. Such resources will be beneficial to spinach breeding efforts for disease resistance in addition to better understanding the virulence mechanisms of this obligate pathogen.