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In BriefIN BRIEF
Open Access

Modulation of Resistance Genes: Two Paths to Alternaria Resistance in Apple

Celine Caseys
Celine Caseys
Department of Plant Sciences, University of California, Davis, California
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  • For correspondence: celcaseys@ucdavis.edu

Published August 2018. DOI: https://doi.org/10.1105/tpc.18.00588

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  • © 2018 American Society of Plant Biologists. All rights reserved.

Apple (Malus × domestica) is a major fruit crop worldwide that faces production losses due to many pathogens. Among them, Alternaria alternata is a fungal pathogen that causes necrotic leaf spots (see figure), defoliation, and moldy fruit cores and constitutes a serious threat to orchards. Different strains of the pathogen with varying pathogenicity and host specificities exist, as determined in part by the fungus’ ability to produce virulence factors, especially cyclic peptide toxins.

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Leaf symptoms in apple trees resistant and susceptible to A. alternata. CK indicates the wild-type cultivar, while A10 is an A6PR antisense line with low levels of sorbitol. Bar = 1 cm. (Reprinted from Meng et al. [2018], Figures 1A and 1B.)

To defend against this pathogen and others, the apple genome encodes many potential paths to resistance. Resistance is largely due to resistance (R) genes. R genes are diverse in their sequences, protein domains, roles, and molecular mechanisms and are essential for mounting an effective defense (Kourelis and van der Hoorn, 2018). Among these, the nucleotide binding/leucine-rich repeat (NLR) proteins perceive specific proteins from the pathogens, leading to induction of a rapid defense response, often culminating in the death of the infected cell. While the number of R genes ranges from ∼200 to 500 in many plant species, the apple genome encodes over a thousand of these resistance genes (Arya et al., 2014). The orchestration of the expression of all these genes in response to specific threats requires complex regulatory networks. Two studies recently published in The Plant Cell describe two independent mechanisms of R gene regulation resulting in resistance to Alternaria alternata in apple.

Plants produce sugars that pathogens crave. Strategically, the internal leaf sugar level in apple is linked to high levels of R gene expression. In this system, more intracellular sugar results in higher resistance to A. alternata. Meng et al. (2018) show that sorbitol, a sugar alcohol that is a major carbon transport form in Rosaceae, including apple, has been co-opted as a signal to regulate the apple R gene MdNLR16. MdNLR16 detects A. alternata by interacting with Hrip1, an effector protein produced by the pathogen. The interaction with the effector protein is a classic gene-for-gene mechanism. Sorbitol-modulated NLR gene expression is controlled by the transcription factor MdWRKY79.

Zhang et al. (2018) describe another path to regulating R genes essential for A. alternata resistance. Apple genomes encode a hairpin RNA, MdhpRNA277, which results in the production of small interfering RNAs that target five R genes (MdRNL1–5). The absence of expression of these R genes results in increased susceptibility to A. alternata. In the resistant cultivars, MdWHy, a transcription factor induced by A. alternata, fails to bind the MdhpRNA277 promoter thanks to a single nucleotide polymorphism in this region. This backfires in the susceptible cultivars, resulting in interference by the plant of its own resistance genes while under attack. This may be an evolutionary misstep, as the hairpin RNA itself may have evolved from a duplication of R genes.

These two studies provide multiple novel and independent potential paths to breeding apple cultivars that are pathogen-resistant by the modulation of R gene expression. It remains to be clarified whether these paths are synergistic or antagonistic in providing resistance to the different strains of A. alternata with and without the host-specific toxins, as used in the two studies, and potentially other fungal pathogens.

Footnotes

  • www.plantcell.org/cgi/doi/10.1105/tpc.18.00588

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References

  1. ↵
    1. Arya, P.,
    2. Kumar, G.,
    3. Acharya, V.,
    4. Singh, A.K.
    (2014). Genome-wide identification and expression analysis of NBS-encoding genes in Malus x domestica and expansion of NBS genes family in Rosaceae. PLoS One 9: e107987.
    OpenUrlCrossRefPubMed
  2. ↵
    1. Kourelis, J.,
    2. van der Hoorn, R.A.L.
    (2018). Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell 30: 285–299.
    OpenUrlAbstract/FREE Full Text
  3. ↵
    1. Meng, D.,
    2. Li, C.,
    3. Park, H.J.,
    4. Gonzalez, J.,
    5. Wang, J.,
    6. Dandekar, A.M.,
    7. Turgeon, B.G.,
    8. Cheng, L.
    (2018). Sorbitol modulates resistance to Alternaria alternata by regulating the expression of an NLR resistance gene in apple. Plant Cell 30: 1562–1581.
    OpenUrlAbstract/FREE Full Text
  4. ↵
    1. Zhang, Q.,
    2. Ma, C.,
    3. Zhang, Y.,
    4. Gu, Z.,
    5. Li, W.,
    6. Duan, X.,
    7. Wang, S.,
    8. Hao, L.,
    9. Wang, Y.,
    10. Wang, S.,
    11. Li, T.
    (2018). A single-nucleotide polymorphism in the promoter of a hairpin RNA contributes to Alternaria alternata leaf spot resistance in apple (Malus × domestica). Plant Cell 30: 1924–1942.
    OpenUrlAbstract/FREE Full Text
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Modulation of Resistance Genes: Two Paths to Alternaria Resistance in Apple
Celine Caseys
The Plant Cell Aug 2018, 30 (8) 1672; DOI: 10.1105/tpc.18.00588

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Modulation of Resistance Genes: Two Paths to Alternaria Resistance in Apple
Celine Caseys
The Plant Cell Aug 2018, 30 (8) 1672; DOI: 10.1105/tpc.18.00588
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The Plant Cell: 30 (8)
The Plant Cell
Vol. 30, Issue 8
Aug 2018
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