Exploring genomic determinants of host specialization in Botrytis cinerea
Botrytis cinerea strains infecting grapevine and tomato display contrasted repertoires of accessory chromosomes, transposons and small RNAs
Recommendation: posted 14 December 2022, validated 15 December 2022
Duplessis, S. (2022) Exploring genomic determinants of host specialization in Botrytis cinerea. Peer Community in Genomics, . https://doi.org/10.24072/pci.genomics.100023
The genomics era has pushed forward our understanding of fungal biology. Much progress has been made in unraveling new gene functions and pathways, as well as the evolution or adaptation of fungi to their hosts or environments through population studies (Hartmann et al. 2019; Gladieux et al. 2018). Closing gaps more systematically in draft genomes using the most recent long-read technologies now seems the new standard, even with fungal species presenting complex genome structures (e.g. large and highly repetitive dikaryotic genomes; Duan et al. 2022). Understanding the genomic dynamics underlying host specialization in phytopathogenic fungi is of utmost importance as it may open new avenues to combat diseases. A strong host specialization is commonly observed for biotrophic and hemi-biotrophic fungal species or for necrotrophic fungi with a narrow host range, whereas necrotrophic fungi with broad host range are considered generalists (Liang and Rollins, 2018; Newman and Derbyshire, 2020). However, some degrees of specialization towards given hosts have been reported in generalist fungi and the underlying mechanisms remain to be determined.
Botrytis cinerea is a polyphagous necrotrophic phytopathogen with a particularly wide host range and it is notably responsible for grey mould disease on many fruits, such as tomato and grapevine. Because of its importance as a plant pathogen, its relatively small genome size and its taxonomical position, it has been targeted for early genome sequencing and a first reference genome was provided in 2011 (Amselem et al. 2011). Other genomes were subsequently sequenced for other strains, and most importantly a gapless assembled version of the initial reference genome B05.10 was provided to the community (van Kan et al. 2017). This genomic resource has supported advances in various aspects of the biology of B. cinerea such as the production of specialized metabolites, which plays an important role in host-plant colonization, or more recently in the production of small RNAs which interfere with the host immune system, representing a new class of non-proteinaceous virulence effectors (Dalmais et al. 2011; Weiberg et al. 2013).
In the present study, Simon et al. (2022) use PacBio long-read sequencing for Sl3 and Vv3 strains, which represent genetic clusters in B. cinerea populations found on tomato and grapevine. The authors combined these complete and high-quality genome assemblies with the B05.10 reference genome and population sequencing data to perform a comparative genomic analysis of specialization towards the two host plants. Transposable elements generate genomic diversity due to their mobile and repetitive nature and they are of utmost importance in the evolution of fungi as they deeply reshape the genomic landscape (Lorrain et al. 2021). Accessory chromosomes are also known drivers of adaptation in fungi (Möller and Stukenbrock, 2017). Here, the authors identify several genomic features such as the presence of different sets of accessory chromosomes, the presence of differentiated repertoires of transposable elements, as well as related small RNAs in the tomato and grapevine populations, all of which may be involved in host specialization. Whereas core chromosomes are highly syntenic between strains, an accessory chromosome validated by pulse-field electrophoresis is specific of the strains isolated from grapevine. Particularly, they show that two particular retrotransposons are discriminant between the strains and that they allow the production of small RNAs that may act as effectors. The discriminant accessory chromosome of the Vv3 strain harbors one of the unraveled retrotransposons as well as new genes of yet unidentified function.
I recommend this article because it perfectly illustrates how efforts put into generating reference genomic sequences of higher quality can lead to new discoveries and allow to build strong hypotheses about biology and evolution in fungi. Also, the study combines an up-to-date genomics approach with a classical methodology such as pulse-field electrophoresis to validate the presence of accessory chromosomes. A major input of this investigation of the genomic determinants of B. cinerea is that it provides solid hints for further analysis of host-specialization at the population level in a broad-scale phytopathogenic fungus.
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The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2022.03.07.483234
Version of the preprint: 2
Author's Reply, 13 Sep 2022
Decision by Sebastien Duplessis, posted 24 May 2022
You will find here two complementary reviews of your manuscript. I concur with both reviewers to acknowledge the quality of the work, analyses and interpretations done; also, the text reads very well and only a few edits are suggested.
As you will see, both reviewers provide suggestions to support further some of your analyses or claims (or eventually to revisit and/or tone down some of said claims).
During my first read, I had questions relating to reviewer 1's comments about the use of the GC% signature. Then after another round, I found the comment of reviewer 2 also very pertinent regarding how the age of TE may affect the quality of mapping, and indeed more precisions about the QC you used would be welcome. Finally, both reviewers propose means for managing their comments which will be helpful to reach a manuscript that could be recommended. I am interested in your answers to the first main comment from reviewer 2. As for the first comment from reviewer 1, I do not know how easy this can be routinely handled in the authors' laboratory?
I am looking forward to reading a revised version of this manuscript and your answers to the constructive comments from these reviewers.
With my best regards.