The Grainger Bioinformatics Center & Negaunee Integrative Research Center, Collections, Conservation and Research Division, The Field Museum, Chicago, IL, 60605, USA.
BMC Genomics. 2024 Oct 26;25(1):1003. doi: 10.1186/s12864-024-10898-8.
The ubiquity of sex across eukaryotes, given its high costs, strongly suggests it is evolutionarily advantageous. Asexual lineages can avoid, for example, the risks and energetic costs of recombination, but suffer short-term reductions in adaptive potential and long-term damage to genome integrity. Despite these costs, lichenized fungi have frequently evolved asexual reproduction, likely because it allows the retention of symbiotic algae across generations. The lichenized fungal genus Lepraria is thought to be exclusively asexual, while its sister genus Stereocaulon completes a sexual reproductive cycle. A comparison of sister sexual and asexual clades should shed light on the evolution of asexuality in lichens in general, as well as the apparent long-term maintenance of asexuality in Lepraria, specifically.
In this study, we assembled and annotated representative long-read genomes from the putatively asexual Lepraria genus and its sexual sister genus Stereocaulon, and added short-read assemblies from an additional 22 individuals across both genera. Comparative genomic analyses revealed that both genera were heterothallic, with intact mating-type loci of both idiomorphs present across each genus. Additionally, we identified and assessed 29 genes involved in meiosis and mitosis and 45 genes that contribute to formation of fungal sexual reproductive structures (ascomata). All genes were present and appeared functional in nearly all Lepraria, and we failed to identify a general pattern of relaxation of selection on these genes across the Lepraria lineage. Together, these results suggest that Lepraria may be capable of sexual reproduction, including mate recognition, meiosis, and production of ascomata.
Despite apparent maintenance of machinery essential for fungal sex, over 200 years of careful observations by lichenologists have produced no evidence of canonical sexual reproduction in Lepraria. We suggest that Lepraria may have instead evolved a form of parasexual reproduction, perhaps by repurposing MAT and meiosis-specific genes. This may, in turn, allow these lichenized fungi to avoid long-term consequences of asexuality, while maintaining the benefit of an unbroken bond with their algal symbionts.
真核生物中无处不在的性行为，由于其高成本，强烈表明它在进化上是有利的。无性谱系可以避免重组的风险和能量成本，但会在短期内降低适应潜力，并对基因组完整性造成长期损害。尽管存在这些成本，地衣真菌经常进化出无性繁殖，这可能是因为它允许共生藻类在几代之间得以保留。地衣真菌属 Lepraria 被认为是完全无性的，而其姊妹属 Stereocaulon 则完成了有性生殖周期。比较姊妹有性和无性谱系应该可以揭示地衣中无性繁殖的进化，以及 Lepraria 中无性繁殖的长期维持，特别是。
在这项研究中，我们组装并注释了来自推测无性的 Lepraria 属及其有性姊妹属 Stereocaulon 的代表性长读基因组，并为这两个属的另外 22 个个体添加了短读基因组组装。比较基因组分析表明，两个属都是异宗配合的，每个属都存在完整的二倍体交配型基因座。此外，我们鉴定并评估了 29 个参与减数分裂和有丝分裂的基因和 45 个有助于形成真菌有性生殖结构（子囊果）的基因。几乎所有 Lepraria 都存在这些基因并且它们似乎具有功能，我们未能确定这些基因在 Lepraria 谱系中选择放松的一般模式。总的来说，这些结果表明 Lepraria 可能具有有性生殖能力，包括配偶识别、减数分裂和子囊果的产生。
尽管存在维持真菌性所必需的机制，但地衣学家经过 200 多年的精心观察，没有发现 Lepraria 中存在典型有性生殖的证据。我们认为 Lepraria 可能已经进化出一种形式的准性生殖，也许是通过重新利用 MAT 和减数分裂特异性基因。这反过来可能使这些地衣真菌避免无性繁殖的长期后果，同时保持与它们的藻类共生体的不间断联系的好处。
