Gastrodia elata BI., a perennial herb of the Gastrodia in the Orchidaceae, has been used in medicine for more than 2,000 years, and is a traditional and valuable Chinese medicine in China (Yuan et al., 2018). G. elata has anticonvulsant, hypnotic, sedative, antidepressant effect and other pharmacological effects (Wu et al., 2023). G. elata to dried rhizomes into medicine, the main medicinal ingredients for gastrodin (Men, Xing, & Guo, 2017). Since G. elata has no roots or leaves and no chloroplasts, it cannot carry out photosynthesis. The growth process of G. elata to Armillaria as the only source of nutrients, through the digestion of Armillaria invasion of rhizomorphs to obtain nutrients (Huang et al., 2019; Yu et al., 2022). And when the Armillaria source of nutrition is insufficient, and will use the nutrients in the body of G. elata for its growth. Therefore, Armillaria and G. elata to establish a special symbiotic relationship (Xu, 2001).
Most terrestrial plants form symbiotic relationships with fungi, and these mycorrhizal fungi can influence soil structure and regulate soil nutrient and carbon cycling (van der Heijden, Martin, Selosse, & Sanders, 2015). Armillaria are one of the most globally important genera of fungal root pathogens and one of the largest and oldest organisms on earth (Baumgartner, Coetzee, & Hoffmeister, 2011) (Smith, Bruhn, & Anderson, 1992). The ability of Armillaria to act as saprophytes, especially white rot fungi, is considered to be beneficial to natural ecosystems because they degrade lignin and therefore play an important role in the carbon cycle (Baumgartner et al., 2011).
Armillaria gallica, an important plant pathogenic fungus, often causes root rot in many trees. However, it is extremely special that Armillaria is an essential fungus in the growth process of G. elata, which can provide nutrients for G. elata. At present, there are more than 70 known species of Armillaria, but only a few Armillaria can be symbiotic with G. elata (Sipos, Anderson, & Nagy, 2018). As the ability of different strains of Armillaria to form rhizomorphs and the ability of rhizomorphs to infest the cortical tissue of G. elata differs, the quality of Armillaria will directly affect the yield of G. elata (Wang et al., 2023). Liu et al. found that the extracellular secretion of pectinase, xylanase, cellulase and laccase and other enzymes not only provide nutrients for the growth and development of A. gallica, but also provide a material basis for A. gallica to infest the epidermis of G. elata (Liu et al., 2019). In other words, the activity of extracellular enzymes of A. gallica is closely related to the yield and quality of G. elata. Meanwhile, Zhao et al. showed that the extracellular enzyme activity was stronger and polysaccharide content was higher in the A. gallica strain (Zhao, Wu, Liu, & Gui, 2022). Moreover, A. gallica mycelium thick, developed, rapid growth, parasitism is weak, is conducive to the cultivation and production of G. elata (Men et al., 2017). A. gallica polysaccharides have a variety of pharmacological activities, including antioxidant effects, anti-fatigue and anti-inflammatory effects (An, Lu, Zhang, Yuan, & Wang, 2017) (Sun et al., 2023) (Wu et al., 2012).
The mitochondrial genome of G. elata was significantly enlarged compared to most other seed plants (Yuan et al., 2018). It was also found that the number of monocotyledonous mannose-binding lectin Gastrodia antifungal protein (GAFP) genes was increased in G. elata, and the GAFP protein could inhibit the growth of ascomycete and basidiomycete, including Armillaria and Ganoderma lucidum, among others (Xu, Liu, Wang, Gu, & Chen, 1998) (Cox, Layne, Scorza, & Schnabel, 2006). Before G. elata established a stable symbiotic relationship with Armillaria, more than 80% of the GAFP genes were highly expressed in protocorms and juvenile tubers (Yuan et al., 2018). Strigolactone promotes Armillaria mycelial branching and contributes to the establishment of a symbiotic relationship between G. elata and Armillaria (Kretzschmar et al., 2012). In G. elata, the number of strigolactone biosynthesis and transport key genes carotenoid cleavage dioxygenases (CCDs) and ABC transporters was increased; the number of calmodulin-dependent protein kinase genes of the does-not-make-infections 3 subfamily (DMI3) genes was also increased, which helped to further regulate the Armillaria colonization in G. elata (Delaux et al., 2012) (Yuan et al., 2018). Tan et al. conducted transcriptome analysis of the symbiotic region of Armillaria and G. elata, and found that the genes for a variety of extracellular enzymes (cellulase, xylanase, laccase) were in a state of down-regulation after Armillaria invaded the endothelial layer of G. elata (Tan et al., 2018). At this time, the infestation of Armillaria on G. elata reached a state of equilibrium, there is no tendency to further invade the G. elata, providing a basis for understanding the symbiotic relationship between Armillaria and G. elata at the level of gene expression.
Currently, studies exploring the symbiotic relationship between Armillaria and G. elata have focused on phenotyping, physiological and biochemical assays, and transcriptome analyses. However, few studies have been reported to explore the symbiotic relationship between Armillaria and G. elata at the genome-wide level. Therefore, carrying out the whole genome analysis of the genus Armillaria is of theoretical significance and applied value for further understanding the role of Armillaria in symbiotic relationship with plants such as G. elata and Polyporus umbellatus. In this study, we present the draft genome of A. gallica M3 strain collected from Xiaocaoba Town, Yiliang County, Zhaotong City, Yunnan Province, and study the genome of A. gallica M3 with 12 other strains of Agaricales. This study helps to analyze the intrinsic mechanism that A. gallica M3 strain can be symbiotic with G. elata at the genomic level, and provides a theoretical basis for the standardization of A. gallica M3 strain accompanied by planting G. elata.