Fungal hybridization confers greater adaptive potential in Verticillium longisporum

Several plant pathogens belong to the genus Verticillium and affect many different plant hosts. Scientists have observed the hybridization of haploid Verticillium species into a stable diploid species, Verticillium longisporum.

A new preprint research paper posted on the bioRxiv* server shows how the hybridization event affected the genome and the transcription profile of Verticillium longisporum. V. longisporum differs from its parents in that it affects only plants of the Brassicaceae family. This is not observed with the parental Verticillium dahlia or other Verticillium species that do not infect Brassica species but have a very broad host range.

Verticillium longisporum displays sub-genome-specific gene expression responses.

Hybridization

Hybridization involves the joining of two different genotypes to form a single genome.

The results of hybridization are a vastly increased ability to adapt, typically conferring increased fitness. On the other hand, the parental genomes may be incompatible in some regions. New species may also emerge, a phenomenon called hybrid speciation.

Despite the rarity of hybridization, most organisms do undergo hybridization at some point due to such compatibility issues. Due to the combination of two complete parental haploid genomes, genome duplication is associated with hybridization in a process called allopolyploidization.

Due to the incompatible parental genomes, the combined genome undergoes "genome shock," resulting in the parental strains undergoing rearrangements of their genomes and gene loss and altered gene expression. Recombination between homeolog genes can give rise to a mosaic structure.

Study aims

The current study explores the impact of the double genomic combination on the adaptation of Verticillium longisporum to its environment that allowed it to become stable and shift its host range.

Mosaic genome structure

The researchers found that the two subgenomes, corresponding to the parental genomes, were mostly composed of mosaic chromosomes, with only two chromosomes of single parental origin in each strain.

The mosaic DNA appears to have arisen mostly from homeologous chromosome rearrangement rather than gene conversion, with 79% of the V. longisporum genes having one homologous copy. Conversely, 97% to 99.6% of genes in each sub-genome occur in a single copy, indicating they are homeologs derived from a single parent.

Mitochondria come from the same parent

The common parent appears to have donated the mitochondrial genomes, which are strikingly almost identical in sequence across the three strains.

Gene deletions cause loss of heterozygosity

Like all hybrids that undergo polyploidy from allogenomic parents, Verticillium longisporum shows a continuing loss of heterozygosity, as has been known, in other hybrids, to be the result of gene conversion or gene loss.

The researchers looked for genes that occurred in a single copy and then examined whether they were encoded in secreted proteins. They found that about 8-10% of these genes encoded such signal peptide-bearing proteins, which is less than expected if the genome carries a homologous copy of the same gene.

They found that single-copy genes occur throughout the two sub-genomes. These may be either due to gene loss or the contribution of one of the parents to the hybrid genome. In this case, they found one or more copies of these single-copy genes in each subgenome of the other strain within the same lineage.

This indicates that the single-copy gene was due to gene deletion, which continues to occur in V. longisporum.

Hybridization increases gene adaptation rate

Comparison of the rate of change in the genes in different subgenomic lineages shows that adaptation is occurring faster in the A1/D3 lineage of V. longisporum than in the A1/D1, within both sub-genomes.

"This may indicate that A1/D3 evolved a longer time under the more relaxes gene evolutionary conditions than A1/D1, i.e. A1 and D3 hybridized a longer time ago than A1/D1." The relaxed gene adaptation does not seem to affect genes with specific functions.

Homogenization of gene expression pattern

Parental gene expression is observed to be differential, preferentially expressed in genes encoding secreted proteins that promote environmental changes. Interestingly, most of these genes show varying profiles of expression at sub-genomic level, when growth conditions are altered.

When differentially expressed gene patterns of the two parental genomes, A1 and D, are compared, the researchers found that higher numbers of differently expressed genes were found in the A1 sub-genome than in the D sub-genomes. This reflects the D parents' later divergence from the ancestral V. dahlia than from the A1 species.

Overall, there is a high correlation between the A1 and D subgenomes' gene expression patterns within this hybrid. This exceeds the correlation between the D genome and the V. dahliae strain JR2. It is also higher compared to the A1 subgenomes between hybridization events or between the JR2 and CQ2 strains of the same species. This indicates that significant homogenization of the subgenomes in V. longisporum occurred with hybridization.

Gene categories express homeologs differentially

Different growing conditions lead to homeolog-specific changes in most V. longisporum genes that express their homeologs differentially. Most of these changes affect genes that encode secreted proteins, which help evade host immunity, intervene in host metabolism, or affect the host's colonization in other ways.

More than half of the differentially expressed homeolog genes in V. longisporum grown in planta have a different expression profile depending on the growing conditions, compared to in vitro growth. This points to sub-genome-specific alterations of gene expression, with a differential homeolog expression as a result.

Such responses specific to the sub-genome level involve genes that participate in multiple metabolic processes.

What are the implications?

Hybrid fungi, therefore, respond to changes in the environment in allele-specific ways, especially when the genes manipulate the environment. Generally, however, gene expression homogenizes following hybridization in fungi.

Genomic rearrangements can occur in many Verticillium species, causing widespread shifting around of chromosomes. In the parental V. dahliae species, such rearrangements especially affect genes that promote host infection and are called dynamic chromosomal regions.

In V. longisporum too, systemic breaks occur in repeat-rich genome regions, since such repetitive sequences are more abundant and therefore likely to provide a substrate for unfaithful repair. This is despite the availability of the two subgenomes in the hybrid nucleus, whereby homeologous sequences are available to provide enough identity for unfaithful repair.

The genome doubling may have conferred faster adaptation rates on the D genome in V. longisporum compared to V. dahliae orthologous genes. This is not a common feature in fungi, with slower genetic change rates in some species after allopolyploidization.

The difference may lie in the environment, with the host range alteration being a possible factor in the higher rate of gene adaptation in V. longisporum. This is not supported by the finding of specifically enriched functional genes among those that showed rapid evolution.

Therefore, with hybridization, V. longisporum acquired plasticity, at both genomic and transcription level, to respond to the environment in a subgenome (parental allele)-specific manner. The presence of two parental genomes also promotes dynamic rearrangement of the genetic material. The outcome may be accelerated gene evolution.

"In comparison to haploid Verticillium species, V. longisporum has a high adaptive potential that can contribute to host immunity evasion and may explain its specialization towards Brassicaceous plant hosts."

*Important Notice

bioRxiv publishes preliminary scientific reports that are not peer-reviewed and, therefore, should not be regarded as conclusive, guide clinical practice/health-related behavior, or treated as established information.

Source:
Dr. Liji Thomas

Written by

Dr. Liji Thomas

Dr. Liji Thomas is an OB-GYN, who graduated from the Government Medical College, University of Calicut, Kerala, in 2001. Liji practiced as a full-time consultant in obstetrics/gynecology in a private hospital for a few years following her graduation. She has counseled hundreds of patients facing issues from pregnancy-related problems and infertility, and has been in charge of over 2,000 deliveries, striving always to achieve a normal delivery rather than operative.

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