Abstract
Downy mildew (DM), caused by obligate parasitic oomycetes, is a destructive disease for a wide range of crops worldwide. Recent outbreaks of impatiens downy mildew (IDM) in many countries have caused huge economic losses. A system to reveal plant–pathogen interactions in the early stage of infection and quickly assess resistance/susceptibility of plants to DM is desired. In this study, we established an early and rapid system to achieve these goals using impatiens as a model. Thirty-two cultivars of Impatiens walleriana and I. hawkeri were evaluated for their responses to IDM at cotyledon, first/second pair of true leaf, and mature plant stages. All I. walleriana cultivars were highly susceptible to IDM. While all I. hawkeri cultivars were resistant to IDM starting at the first true leaf stage, many (14/16) were susceptible to IDM at the cotyledon stage. Two cultivars showed resistance even at the cotyledon stage. Histological characterization showed that the resistance mechanism of the I. hawkeri cultivars resembles that in grapevine and type II resistance in sunflower. By integrating full-length transcriptome sequencing (Iso-Seq) and RNA-Seq, we constructed the first reference transcriptome for Impatiens comprised of 48,758 sequences with an N50 length of 2060 bp. Comparative transcriptome and qRT-PCR analyses revealed strong candidate genes for IDM resistance, including three resistance genes orthologous to the sunflower gene RGC203, a potential candidate associated with DM resistance. Our approach of integrating early disease-resistance phenotyping, histological characterization, and transcriptome analysis lay a solid foundation to improve DM resistance in impatiens and may provide a model for other crops.
Highlights
Downy mildew (DM) is a destructive disease caused by obligate parasitic oomycetes from the Peronosporaceae family[1]
All plants died before February 16, 2015 (256 DAP), indicating all these I. walleriana cultivars are highly susceptible to impatiens downy mildew (IDM)
Candidate genes were first mined based on the following criteria: (1) differentially expressed (FDR < 0.05, fold change ≥ 2) for Divine Orange Bronze Leaf” (DOB) cotyledon (S) vs DOB-true leaf (R); (2) within the same tissue type, for the genes upregulated in DOB-true leaf (R) compared with DOB cotyledon (S), we looked for those that were expressed at higher levels (FDR < 0.05, fold change ≥2) in IDM-resistant cultivars than in susceptible cultivars; (3) for the genes downregulated in DOB-true leaf (R) compared with DOB cotyledon (S), we looked for those that were expressed at lower levels (FDR < 0.05, fold change ≥2) in resistant cultivars than in susceptible cultivars (Table 4 and Supplementary Table S10)
Summary
Downy mildew (DM) is a destructive disease caused by obligate parasitic oomycetes from the Peronosporaceae family[1] It has been a serious challenge for a wide range of cultivated crops including row crops, vegetables, Peng et al Horticulture Research (2021)8:108 races with higher virulence levels emerge constantly, resulting in fungicide resistance in DM pathogens and severely hindering the effectiveness of fungicides whose development could take many years and cost hundreds of millions of dollars[6,7]. The common DM species infecting horticultural crops include Peronospora destructor (onion), Peronospora belbahrii (basil), Plasmopara viticola (grape), Pseudoperonospora cubensis (cucurbits), Plasmopara halstedii (sunflower), Peronospora effusa (spinach), and Bremia lactucae (lettuce) To combat this disease, host resistance to DM has been identified in several crops and a few resistance genes have been cloned. The sunflower genome contains more than 30 DM resistance genes distributed in the domesticated and wild species[9]
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