A complex resistance locus in Solanum americanum recognizes a conserved Phytophthora effector

Witek, Kamil; Lin, Xiao; Karki, Hari S.; Jupe, Florian; Witek, Agnieszka; Steuernagel, Burkhard; Stam, Remco; Oosterhout, Cock van; Fairhead, Sebastian; Heal, Robert; Cocker, Jonathan M.; Bhanvadia, Shivani; Barrett, William L.; Wu, Chih-Hang John; Adachi, Hiroaki; Song, Tianqiao; Kamoun, Sophien; Vleeshouwers, Vivianne G. A. A.; Tomlinson, Laurence; Wulff, Brande B. H.; Jones, Jonathan D. G.

doi:10.1038/s41477-021-00854-9

Cited by 66 publications

(71 citation statements)

References 71 publications

(52 reference statements)

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“…To identify Avramr1, we tested 278 available RXLR effectors (Table S1) by coexpressing them with Rpi-amr1-2273 in Nicotiana benthamiana (Rietman, 2011). Rpi-amr1-2273 (hereafter Rpi-amr1) is a functional Rpi-amr1 homolog cloned from S. americanum SP2273 (Witek et al, 2020). However, we did not identify an effector that activated Rpi-amr1-dependent hypersensitive response (HR) from the available RXLR effector libraries and concluded these libraries are incomplete.…”

Section: Available Recombinant Rxlr Effector Libraries Do Not Contain Avramr1mentioning

confidence: 89%

“…The effectors were synthesized, cloned into an expression vector with CaMV 35S promoter, and transformed into Agrobacterium GV3101-pMP90 for agroinfiltration in N. benthamiana (Figure 4a). All the effectors were infiltrated alone or coinfiltrated with Rpi-amr1 (Witek et al, 2020). Among the 47 effectors, PITG_07569 was the only effector that triggered an HR when coexpressed with Rpi-amr1.…”

Section: Identification Of Avramr1mentioning

confidence: 99%

“…Two Rpi genes encoding NLR proteins, Rpi-amr3 and Rpi-amr1, were cloned from S. americanum and confer late blight resistance in potato (Witek et al, 2016(Witek et al, , 2020.…”

mentioning

confidence: 99%

“…Here, to identify the recognized effector of the newly cloned Rpi-amr1 protein from S. americanum (Witek et al, 2020), we screened all currently available RXLR effectors for recognition but without success. Therefore, we adapted and improved PenSeq with long read (PacBio) and cDNA sequencing, and extended the list of candidate effectors that could be screened.…”

mentioning

confidence: 99%

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Identification ofAvramr1fromPhytophthora infestansusing long read and cDNA pathogen-enrichment sequencing (PenSeq)

Lin

Song

Fairhead

et al. 2020

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1 2 • Potato late blight, caused by the oomycete pathogen Phytophthora infestans, 3 significantly hampers potato production. Recently, a new Resistance to Phytophthora 4 infestans (Rpi) gene, Rpi-amr1, was cloned from a wild Solanum species, Solanum 5 americanum. Identification of the corresponding recognized effector (Avirulence, or 6Avr) genes from P. infestans is key to elucidating their naturally occurring sequence 7 variation, which in turn informs the potential durability of the cognate late blight 8 resistance. 9• To identify the P. infestans effector recognized by Rpi-amr1, we screened available 10 effector libraries and used long read and cDNA pathogen-enrichment sequencing 11 (PenSeq) on four P. infestans isolates to explore the untested effectors. 12• By using SMRT and cDNA PenSeq, we identified 47 highly expressed effectors from 13 P. infestans, including PITG_07569 which triggers a highly specific cell death response 14 when transiently co-expressed with Rpi-amr1 in Nicotiana benthamiana, suggesting 15 that PITG_07569 is Avramr1. 16• Here we demonstrate that long read and cDNA PenSeq enables the identification of 17 full-length RxLR effector families, and their expression profile. This study has revealed 18 key insights into the evolution and polymorphism of a complex RxLR effector family 19 that is associated with the recognition by Rpi-amr1.

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Section: Available Recombinant Rxlr Effector Libraries Do Not Contain Avramr1mentioning

confidence: 89%

Section: Identification Of Avramr1mentioning

confidence: 99%

“…Two Rpi genes encoding NLR proteins, Rpi-amr3 and Rpi-amr1, were cloned from S. americanum and confer late blight resistance in potato (Witek et al, 2016(Witek et al, , 2020.…”

mentioning

confidence: 99%

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confidence: 99%

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Identification ofAvramr1fromPhytophthora infestansusing long read and cDNA pathogen-enrichment sequencing (PenSeq)

Lin

Song

Fairhead

et al. 2020

Preprint

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“…Genes encoding nucleotide-binding domain leucine-rich repeat-containing proteins (NLR) are one example of major resistance genes. NLR genes have been studied in natural plant populations and are reported to be diverse at the genetic level (Stam et al ., 2019a, Van de Weyer et al ., 2019; Witek et al ., 2021). Similarly, members of the receptor-like proteins (RLPs) family show intraspecific variation in the presence-absence of defence responses or variability in expression patterns of these genes (Van der Hoorn et al ., 2001; Kruijt et al ., 2005; Kahlon et al ., 2020, Steidele and Stam, 2020).…”

Section: Introductionmentioning

confidence: 99%

Laminarin-triggered defence responses are geographically dependent for natural populations ofSolanum chilense

Kahlon

Förner

Muser

et al. 2021

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Natural plant populations are highly polymorphic and often show intraspecific quantitative, variation in resistance properties against pathogens. The activation of the underlying defence responses can depend on the perception of conserved pathogen-associated molecular patterns (PAMPs). To dissect and understand such variation, we evaluated the diversity of responses induced by laminarin (representing a general glucan elicitor of plant immune responses) in the wild tomato species Solanum chilense. We confirm considerable overlap of the plant's global transcriptional responses to laminarin and to the oomycete pathogen Phytophthora infestans. We further measured key components of basal defence responses such as reactive oxygen species (ROS) production and levels of diverse phytohormones and their derivatives upon elicitation with laminarin in 83 plants originating from nine natural populations of S. chilense from distinct geographic origin. We found high diversity in these components at basal and elicitor-induced levels. We generated generalised linear mixed models (GLMMs) with these components to explain the observed resistance phenotype against P. infestans in the plants and found that additive effects of multiple components best explain resistance at the species level. For individual components, we observed the strongest positive correlation between the resistance phenotype and ethylene (ET) production upon laminarin elicitation. The strength of this correlation differed between individual populations. Chemical inhibition of ET production in individuals from a population, in which ET production was associated with resistance, provoked more severe disease symptoms. Our findings reveal high diversity in the strength of induced defence responses within a species and in the basal levels of other stress-related phytohormones. We show the involvement of multiple components with a quantitatively different contribution of individual components to resistance in geographically separated populations of S. chilense against P. infestans.

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Anti‐oomycete ability of scopolamine against Phytophthora infestans, a terrible pathogen of potato late blight

et al. 2023

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BACKGROUNDPhytophthora infestans causes late blight, threatening potato production. The tropane alkaloid scopolamine from some industrial plants (Datura, Atropa, etc.) has a broad‐spectrum bacteriostatic effect, but its effect on P. infestans is unknown.RESULTSIn the present study, scopolamine inhibited the mycelial growth of phytopathogenic oomycete P. infestans, and the half‐maximal inhibitory concentration (IC50) was 4.25 g L−1. The sporangia germination rates were 61.43%, 16.16%, and 3.99% at concentrations of zero (control), 0.5 IC50, and IC50, respectively. The sporangia viability of P. infestans was significantly reduced after scopolamine treatment through propidium iodide and fluorescein diacetate staining, speculating that scopolamine destroyed cell membrane integrity. The detached potato tuber experiment demonstrated that scopolamine lessened the pathogenicity of P. infestans in potato tubers. Under stress conditions, scopolamine showed good inhibition of P. infestans, indicating that scopolamine could be used in multiple adverse conditions. The combination effect of scopolamine and the chemical pesticide Infinito on P. infestans was more effective than the use of scopolamine or Infinito alone. Moreover, transcriptome analysis suggested that scopolamine leaded to a downregulation of most P. infestans genes, functioning in cell growth, cell metabolism, and pathogenicity.CONCLUSIONTo our knowledge, this is the first study to detect scopolamine inhibitory activity against P. infestans. Also, our findings highlight the potential of scopolamine as an eco‐friendly option for controlling late blight in the future. © 2023 Society of Chemical Industry.

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A complex resistance locus in Solanum americanum recognizes a conserved Phytophthora effector

Cited by 66 publications

References 71 publications

Identification ofAvramr1fromPhytophthora infestansusing long read and cDNA pathogen-enrichment sequencing (PenSeq)

Identification ofAvramr1fromPhytophthora infestansusing long read and cDNA pathogen-enrichment sequencing (PenSeq)

Laminarin-triggered defence responses are geographically dependent for natural populations ofSolanum chilense

Anti‐oomycete ability of scopolamine against Phytophthora infestans, a terrible pathogen of potato late blight

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