Comparative transcriptomics unravels new genes imparting scab resistance in apple (Malus x domestica Borkh.)

Masoodi, Khalid Z.; Ahmed, Nazeer; Mir, Mudasir Ahmad; Bhat, Basharat Ahmad; Shafi, Afshana; Mansoor, Sheikh; Rasool, Rovidha Saba; Yaseen, Mıfftha; Dar, Zahoor Ahmad; Mir, Javid Iqbal; Andrabi, Syed Mudasir; Ganai, Nazir Ahmad

doi:10.1007/s10142-022-00889-x

Cited by 11 publications

(6 citation statements)

References 56 publications

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“…In our study, we analyzed the differences in the transcriptome of N. benthamiana before and after virus inoculation, and the 5046 identified DEGs, which were previously identified as TMV resistance-related genes, such as glutathione S-transferase (Gullner et al 1999 ; Künstler et al 2019 ; Masoodi et al 2022 ), PR1 , and PR2 (Cornelissen et al 1986 ; Wang et al 2013 ), were among the most upregulated genes (Fig. 1 and Supplementary Table S1 ).…”

Section: Discussionmentioning

confidence: 99%

Identification and characterization of TMV-induced volatile signals in Nicotiana benthamiana: evidence for JA/ET defense pathway priming in congeneric neighbors via airborne (E)-2-octenal

Hong

Zheng

Cheng

et al. 2023

Funct Integr Genomics

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Plants release a mixture of volatile compounds when subjects to environmental stress, allowing them to transmit information to neighboring plants. Here, we find that Nicotiana benthamiana plants infected with tobacco mosaic virus (TMV) induces defense responses in neighboring congeners. Analytical screening of volatiles from N. benthamiana at 7 days post inoculation (dpi) using an optimized SPME–GC–MS method showed that TMV triggers the release of several volatiles, such as (E)-2-octenal, 6-methyl-5-hepten-2-one, and geranylacetone. Exposure to (E)-2-octenal enhances the resistance of N. benthamiana plants to TMV and triggers the immune system with upregulation of pathogenesis-related genes, such as NbPR1a, NbPR1b, NbPR2, and NbNPR1, which are related to TMV resistance. Furthermore, (E)-2-octenal upregulates jasmonic acid (JA) that levels up to 400-fold in recipient N. benthamiana plants and significantly affects the expression pattern of key genes in the JA/ET signaling pathway, such as NbMYC2, NbERF1, and NbPDF1.2, while the salicylic acid (SA) level is not significantly affected. Our results show for the first time that the volatile (E)-2-octenal primes the JA/ET pathway and then activates immune responses, ultimately leading to enhanced TMV resistance in adjacent N. benthamiana plants. These findings provide new insights into the role of airborne compounds in virus-induced interplant interactions.

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Section: Discussionmentioning

confidence: 99%

Identification and characterization of TMV-induced volatile signals in Nicotiana benthamiana: evidence for JA/ET defense pathway priming in congeneric neighbors via airborne (E)-2-octenal

Hong

Zheng

Cheng

et al. 2023

Funct Integr Genomics

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“…In addition, nuclear proteome analysis identified 13 proteins with differential expression patterns among varying scab resistance 'Antonovka' accessions (Sikorsskaite-Gudziuniene et al, 2017). Recently, Masoodi et al (Masoodi et al, 2022) performed a RNA-seq analyze comparing three scab-resistant ('Florina', 'Prima', and 'White Dotted Red') and three susceptible ('Ambri', 'Vista Bella', and 'Red Delicious') apple genotypes out to mine new scab resistance genes. They reported the modulation of expression of 822 genes related to various pathways, i.e., metabolic, protein processing, biosynthesis of secondary metabolites, plant hormone signal transduction, autophagy, ubiquitin-mediated proteolysis, plantpathogen interaction, lipid metabolism, and protein modification pathways.…”

Section: Introductionmentioning

confidence: 99%

“…Thus, if large-scale analyses of pear and apple scab host resistance can be found, in-depth knowledge of transcriptional patterns and gene functions involved in apple and pear scab nonhost resistance is still needed. The objectives of our study were 1) to precisely describe nonhost resistance symptoms in M. domestica / V.pyrina and P. communis / V. inaequalis interactions 2) to analyze the underlying molecular mechanisms of both nonhost interactions through a transcriptomic study 3) to compare the mechanism of host (Perchepied et al, 2021, Masoodi et al, 2022 and nonhost scab resistance in apple and European pear.…”

Section: Introductionmentioning

confidence: 99%

Phenotypic and transcriptomic analyses reveal major differences between apple and pear scab nonhost resistance

Vergne¹,

Chevreau²,

Ravon³

et al. 2023

Peer Community Journal

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Nonhost resistance is the outcome of most plant/pathogen interactions, but it has rarely been described in Rosaceous fruit species. Apple (Malus x domestica Borkh.) have a nonhost resistance to Venturia pyrina, the scab species attacking European pear (Pyrus communis L.). Reciprocally, P. communis have a nonhost resistance to Venturia inaequalis, the scab species attacking apple. The major objective of our study was to compare the scab nonhost resistance in apple and in European pear, at the phenotypic and transcriptomic levels. Macro-and microscopic observations after reciprocal scab inoculations indicated that, after a similar germination step, nonhost apple/V. pyrina interaction remained nearly symptomless, whereas more hypersensitive reactions were observed during nonhost pear/V. inaequalis interaction. Comparative transcriptomic analyses of apple and pear nonhost interactions with V. pyrina and V. inaequalis, respectively, revealed differences. Very few differentially expressed genes were detected during apple/V. pyrina interaction, preventing the inferring of underlying molecular mechanisms. On the contrary, numerous genes were differentially expressed during pear/V. inaequalis interaction, allowing a deep deciphering. Pre-invasive defense, such as stomatal closure, could be inferred, as well as several post-invasive defense mechanisms (apoplastic reactive oxygen species accumulation, phytoalexin production and alterations of the epidermis composition). In addition, a comparative analysis between pear scab host and nonhost interactions indicated that, although specificities were observed, two major defense lines seems to be shared in these resistances: cell wall and cuticle potential modifications and phenylpropanoid pathway induction. This first deciphering of the molecular mechanisms underlying a nonhost scab resistance in pear offers new possibilities for the genetic engineering of sustainable scab resistance in this species. Concerning nonhost scab resistance in apple, further analyses must be considered with the aid of tools adapted to this resistance with very few cells engaged.

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“…In addition, nuclear proteome analysis identified 13 proteins with differential expression patterns among varying scab resistance ‘Antonovka’ accessions [22]. Recently, Masoodi et al [23] performed a RNA-seq analyze comparing three scab-resistant (‘Florina’, ‘Prima’, and ‘White Dotted Red’) and three susceptible (‘Ambri’, ‘Vista Bella’, and ‘Red Delicious’) apple genotypes out to mine new scab resistance genes. They reported the modulation of expression of 822 genes related to various pathways, i.e., metabolic, protein processing, biosynthesis of secondary metabolites, plant hormone signal transduction, autophagy, ubiquitin-mediated proteolysis, plant-pathogen interaction, lipid metabolism, and protein modification pathways.…”

Section: Introductionmentioning

confidence: 99%

“…The objectives of our study were 1) to precisely describe nonhost resistance symptoms in M. domestica / V . pyrina and P. communis / V. inaequalis interactions 2) to analyze the underlying molecular mechanisms of both nonhost interactions through a transcriptomic study 3) to compare the mechanism of host (Perchepied et al ., 2021, Masoodi et al ., 2022) and nonhost scab resistance in apple and European pear.…”

Section: Introductionmentioning

confidence: 99%

Phenotypic and transcriptomic analyses reveal major differences between apple and pear scab nonhost resistance

Vergne

Chevreau

Ravon

et al. 2021

Preprint

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Background: Nonhost resistance is the outcome of most plant/pathogen interactions, but it has rarely been described in Rosaceous fruit species. Apple (Malus x domestica Borkh.) is a nonhost for Venturia pyrina, the scab species attacking European pear (Pyrus communis L.). Reciprocally, P. communis is a nonhost for Venturia inaequalis, the scab species attacking apple. The major objective of our study was to compare the scab nonhost resistance in apple and in European pear, at the phenotypic and transcriptomic levels. Results: Macro- and microscopic observations after reciprocal scab inoculations indicated that, after a similar germination step, nonhost apple/V. pyrina interaction remained nearly symptomless, whereas hypersensitive reactions were observed during nonhost pear/V. inaequalis interaction. Comparative transcriptomic analyses of apple and pear nonhost interactions with V. pyrina and V. inaequalis, respectively, revealed considerable differences. Very few differentially expressed genes were detected during apple/V. pyrina interaction, which is consistent with a symptomless type I nonhost resistance. On the contrary, numerous genes were differentially expressed during pear/V. inaequalis interaction, as expected in a type II nonhost resistance involving visible hypersensitive reaction. Pre-invasive defense, such as stomatal closure, was detected, as well as several post-invasive defense mechanisms (apoplastic reactive oxygen species accumulation, phytoalexin production and alterations of the epidermis composition). In addition, a comparative analysis between pear scab host and nonhost interactions indicated that, although specificities were observed, two major defense lines were shared in these resistances: cell wall and cuticle modifications and phenylpropanoid pathway induction. Conclusion: This first deciphering of the molecular mechanisms underlying a nonhost scab resistance in pear offers new possibilities for the genetic engineering of sustainable scab resistance in this species.

show abstract

Comparative transcriptomics unravels new genes imparting scab resistance in apple (Malus x domestica Borkh.)

Cited by 11 publications

References 56 publications

Identification and characterization of TMV-induced volatile signals in Nicotiana benthamiana: evidence for JA/ET defense pathway priming in congeneric neighbors via airborne (E)-2-octenal

Identification and characterization of TMV-induced volatile signals in Nicotiana benthamiana: evidence for JA/ET defense pathway priming in congeneric neighbors via airborne (E)-2-octenal

Phenotypic and transcriptomic analyses reveal major differences between apple and pear scab nonhost resistance

Phenotypic and transcriptomic analyses reveal major differences between apple and pear scab nonhost resistance

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