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Review Mucoromycota: going to the roots of plant-interacting fungi

Paola BONFANTE*, Francesco VENICE

Department of Life Science and Systems Biology, University of Torino, Italy article info abstract

Article history: Many fungi (from micro-to macromycetes) interact with plants as a relevant component of Received 2 October 2019 plant microbiota. The aim of the review is to focus on the early diverging fungi (Mucoromy- Received in revised form cota) whose members establish a wide range of beneficial or pathogenic interactions with 10 December 2019 their green hosts, depending on their phylogenetic position. While Mortierellomycotina are Accepted 11 December 2019 mostly identified as rhizospheric microbes, Glomeromycotina are acknowledged as the most widespread arbuscular mycorrhizal fungi, leading to the establishment of an ancient Keywords: and ecologically relevant symbiosis with plants. A combination of data from fossils and Arbuscular mycorrhizal symbiosis from novel observations demonstrates how the third subphylum, Mucoromycotina, is a Early diverging fungi source of so far largely unidentified plant-interacting fungi. In addition to pathogens, other Evolution members establish symbiosis with non-vascular plants, Gymnosperms and Angiosperms Genome sequences producing both ecto- and endomycorrhizas. Plant-interacting fungi A survey of the so far sequenced genomes illustrates how these fungi share some genetic traits, mirroring their common origin, while other features are specific for each group. In addition to some shared phenotypic traits (aseptate hyphae, multinuclear conditions) en- dobacteria belonging to the group of Burkholderia-related and to the Mycoplasma-related bacteria are present in many members of the three subphyla, suggesting that the common ancestor was already hosting endobacteria. The review also underlines some idiosyn- crasies mostly due to the lack of fossil reports which may confirm phylogenomics as well as the still limited functional data. ª 2019 British Mycological Society. Published by Elsevier Ltd. All rights reserved.

1. Introduction are around 400,000 plant species including relatively few spe- cies from Bryophytes, Ferns and Gymnosperms, and the Microscopic entities or giants, friends or killers, degraders or dominating Angiosperms: they are present in all the environ- producers, fungi play crucial roles for the life on our planet. ments and have an impact on all the aspects of our society, Among the many relevant actions they do, one of the most ensuring oxygen, food, textile, medicines for the whole hu- important in the ecological context is their capacity to interact manity. However, current knowledge tells us that most of with the green inhabitants of the earth. According to the Plant these plants live interacting with fungi, which represent a State of World 2017 (https://stateoftheworldsplants.org), there relevant component of their microbiota (Bonfante et al.,

* Corresponding author. E-mail address: [email protected] (P. Bonfante). https://doi.org/10.1016/j.fbr.2019.12.003 1749-4613/ª 2019 British Mycological Society. Published by Elsevier Ltd. All rights reserved.

Please cite this article as: Bonfante, P., Venice, F., Mucoromycota: going to the roots of plant-interacting fungi, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.003 2 P. Bonfante, F. Venice

2019). Even if fungi are grouped inside 144,000 species named small animals and of other fungi, i.e. mycoparasites, Mucoro- and classified, according to the Fungal State of the World mycota with their three subphyla (Glomeromycotina, Mortier- (https://stateoftheworldsfungi.org/2018/reports/SOTWFun- ellomycotina and Mucoromycotina) group species of gi_2018_Full_Report.pdf2018), it is estimated that their vast mycorrhizal fungi, root endophytes, plant pathogens and majority (over 93%) is currently unknown, leading to the sug- many decomposers of plant material (Fig. 1). gestion that fungal species could be between 2.2 and 3.8 million (Hawksworth and Lucking,€ 2017). This number sug- Glomeromycotina gests the remarkable fungal/plant species ratio of 7/1. Notwithstanding this immense diversity, rapid advances in Glomeromycotina are the iconic representative of arbuscular DNA sequencing technologies are allowing us to uncover the mycorrhizal (AM) fungi, but interestingly enough they also major steps in fungal evolution and to understand how the embrace Geosiphon pyriformis, a very rare fungus which associ- fungal tree of life crosses the plant tree. Both plants and fungi ates with a cyanobacterium (Schußler,€ 2012). The phyloge- have lived a transition from an aquatic environment to the netic position of AM fungi has been an enigma for years emerged lands: plants are hypothesized to have colonized (Koide and Mosse, 2004; Schubler et al., 2001; Bonfante, 2018) lands as early as 700 million years ago, when the Earth’s sur- and their ranking, Glomeromycota vs Glomeromycotina face already hosted cyanobacteria, algae and fungi, but well (Spatafora et al. 2016, Tedersoo et al. 2018) is still controver- conserved plant fossils date back about 470 million years sial. However, their assignment to Mucoromycota well recon- ago and belong to early vascular plants (Taylor et al., 2009). Ac- ciles morphological observations (they are aseptate and cording to the spectacular discoveries by Kidston and Lang multinucleated fungi as Mortierella or Rhizopus), and also en- (1917) done in the Rhynie Chert, these first plants, as Aglaophy- lightens their unique features: they are obligate symbionts, ton major, were described as around 18 cm tall, with cylindrical meaning that they live in the soil forming a network of hy- prostrate axes lying on the substrates and functioning as rhi- phae, but largely depend on the reduced carbon obtained by zomes. By contrast, convincing fossils assigned to liverworts, the host plants; on the other hand they provide plants with which are considered the early plants which have colonized minerals thanks to the establishment of intimate cellular con- lands, have been found only in later times, for example in tacts (Lanfranco et al., 2018). Glomeromycotina which contain Cenozoic amber (Taylor et al., 2009). Interestingly, the fossils different orders (Archaeosporales, Diversisporales, Glomer- of fungi tell us a parallel story: it has been suggested that fungi ales, and Paraglomerales), interact with a huge number of may have diverged from metazoans more than 1 billion years plants: liverworts, ferns, gymnosperms (from Ginkgo biloba to ago (Samarakoon et al., 2017), but again the most important Cupressus) and angiosperms (from trees such as poplar and ap- source of ancient fungi is the early Devonian Rhynie Chert, ple trees to herbs and shrubs). The largest Angiosperm plant where hyphae and spores have been detected from the silici- families, as Asteraceae, Fabaceae, Rubiaceae and Poaceae fied matrix and from tissues of plants such as A. major (Taylor with more than 32,000, 20,000, 13,000 and 11,000 species, et al., 2009). For their morphological features, these ancient respectively, are predominantly good hosts for AM fungi. fungi have been mostly identified as related to the fungi which The crops selected by the green revolution and which feed are today classified as Glomeromycotina and Chytridiomycota the 80% of the current humanity are again hosts for AM fungi (Spatafora et al., 2016). Even if one of the first Ascomycota fos- (from rice and potato to cassava and tomato). Since many of sil reports has been identified in the Rhynie Chert, most of the them are also model plants, molecular and cell biology studies other reports for Dikarya (which group Asco- and Basidiomy- mostly based on mutant availability are offering exciting de- cota) have been found in amber dating back to more recent scriptions of the plant/Glomeromycotina interactions. The times (Taylor et al., 2009). Dikarya offer the highest fungal di- current resulting picture is mostly a plant-centered view, versity which is also mirrored by a large wealth of information where - with few exceptions - the game is played by the plant on their origin, ecology and reproductive traits as well on their host. The scheme (Fig. 2) summarizes many of the plant check phylogenetic placement (Schoch et al., 2009; Zhao et al., 2017, points which control the AM colonization (Pimprikar and Hibbett et al., 2018). Gutjahr, 2018). On the basis of the scenario offered by fossils, Glomeromy- cotina and other Mucoromycota seem to be the most ancient Mortierellomycotina fungi which evolved to interact with plants. The aim of the re- view is to focus on the Mucoromycota and to understand Mortierellomycotina, with the single order of Mortierellales, whether data from omics approaches support a common consists of many saprobic species, but the most recent meta- evolutionary history for these so diverse fungi. barcoding researches based on environmental samplings reveal a strong diversity with many taxa associated to rhizo- sphere and plants roots, where they live as endophytes 2. Mucoromycota: a look at their position in (Nagy et al., 2011; Shakya et al., 2013; Summerbell, 2005). the fungal tree of life Liao et al. (2019) demonstrated how Mortierella elongata elicits a wide range of gene expression responses in poplar, including An accurate phylogenomics analysis has revealed that the defense system manipulation. However, cytological observa- early diverging fungi which were once referred as Zygomy- tions revealing a physical connectivity between the fungal hy- cetes, can now be grouped in two phyla, Mucoromycota and phae and cell roots are not yet available. By contrast, the Zoopagomycota (Spatafora et al., 2016). While the latter taxon exciting observation that M. elongata may associate with the contains species that are primarily parasites and pathogens of alga Nannochloropsis oceanica causing the algal aggregation

Please cite this article as: Bonfante, P., Venice, F., Mucoromycota: going to the roots of plant-interacting fungi, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.003 The roots of plant-interacting fungi 3

Plant- and Bacteria InteracƟng Mucoromycota

MucoromycoƟna MorƟerellomycoƟna GlomeromycoƟna

Mucorales Endogonales MorƟerellales AM Fungi Geosiphonales

Jimgerdemannia Rhizopus microsporus Densospora MorƟerella elongata Rhizophagus, Gigaspora Geosiphon pyriforme Endogone - Endophyte -Saprotroph - Mycorrhizal - Living in the - OpportunisƟc detected - Ectomycorrhizal -Endophyte - Obligate biotrophs soil pathogen in Bryophytes, - Saprotroph - Host for - Present in 80% -SymbioƟc - Host for Ferns, Lycophytes, - Host for endobacteria, of land plants with endobacteria, Trifolium endobacteria, MRE, BRE type, - Hosts for Cyanobacteria BRE type - Host for MRE type Algae endobacteria Host for endobacteria, MRE, endobacteria. MRE type BRE type MRE type

Fig. 1 e The scheme summarizes the current knowledge on the Mucoromycota which interact with plants (as pathogens, symbionts or endophytes) and bacteria. The taxonomic organization of Mucoromycota in three subphyla is based on Spatafora et al. (2016), while the listed biological traits derive from the researches illustrated in the text. The endobacteria are identified as Burkholderia-related (BRE), Mycoplasma-related (MRE) and Cyanobacteria and are illustrated with a different color code.

and lastly allowing the algal colonization (Du et al., 2019), interactions, Endogonales are surely the most interesting demonstrates that - at least under laboratory conditions e and intriguing order (Hoysted et al., 2018). They embrace fungi the fungus can interact with photosynthetic organisms, open- which behave as saprobes, ectomycorrhizal, and arbuscules- ing the room for further studies of experimental evolution. M. producing fungi. The capacity of Endogone lactiflua (now Jimger- elongata and N. oceanica may offer a parallel with the Glomer- demannia lactiflua; Desiro et al., 2017) to support ectomycorrhi- omycotina G. pyriformis which contains a cyanobacterium zae with pine seedlings was first reported by Fassi et al. (1969), (Schußler,€ 2012), originating therefore a photosynthetic or- while Bonfante and Scannerini (1977) obtained Endogone ecto- ganism, which is present in nature. Therefore, in one hand mycorrhizae in microcosms, describing their morphological the first couple is the product of biosynthetic biology, while features, and illustrating how the fungus can develop some the second is a natural association, but in both the examples intracellular hyphae. Molecular analyses confirmed the Endo- there is a fungus which acquires photosynthetic capacities gonales nature of some ectomycorrhizae originating from thanks to a symbiosis with an alga or a cyanobacterium. different environments (Tedersoo et al., 2010; Tedersoo and Smith, 2013; Yamamoto et al., 2017). Bidartondo et al. (2011) Mucoromycotina were the first to report how fungi related to Endogonales could colonize ferns and liverworts with an endophytic style, sug- Mucoromycotina consists of three orders: Endogonales, gesting that non-seed plants could benefit from this interac- Mucorales and Umbelopsidales and has a huge number of spe- tion which offered an alternative fungal option to the more cies including model fungi, such as Mucor mucedo and Phyco- successful AM fungi. Strullu-Derrien et al. (2014) re- myces blakesleeanus, as well as industrially important species investigated Rhynie Chert materials and indeed fungal struc- as Rhizopus. Mucorales also contain plant pathogen members, tures belonging to two endophytes related to the today Mucor- such as R. microsporus which harbors the beta-proteobacteria omycotina and Glomeromycotina could be detected in the Burkholderia rhizoxinica and B. endofungorum (Partida-Martinez corm of Horneophyton lignieri. This is an interesting extinct et al., 2007), currently renamed to Mycetohabitans rhizoxinica early plant which is located between the hornworts and the and M. endofungorum (Estrada de Los Santos et al., 2018). Bacte- Rhyniopsida for its characteristic features. Many experiments rial endosymbionts provide the fungus with potent toxins and from the group of Katie Field have demonstrated the function- regulate both its asexual and sexual reproduction, making R. ality of the interaction supported by Mucoromycotina which microsporus an attractive system to study fungal interactions release P and N to their liverwort hosts (Field et al., 2016, with bacteria (see below) and to decipher reproductive biology 2015; Field and Pressel, 2018). Furthermore, Orchard et al. of Mucoromycotina (Partida-Martinez et al., 2007a; Mondo (2017) suggested that the so-called Glomus tenuis has to be et al., 2017). However, in the context of plant/fungal looked as belonging to Mucoromycotina on the basis of

Please cite this article as: Bonfante, P., Venice, F., Mucoromycota: going to the roots of plant-interacting fungi, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.003 4 P. Bonfante, F. Venice

Fig. 2 e Many studies have described the molecular mechanisms underlying the colonization process of AM fungi with the identification of plant and fungal bioactive molecules which allow partner recognition as well as the plant genes which control the recognition phase (Common symbiotic pathway genes), and the further steps of the fungal colonization. The plant genes, associated to the different steps of the colonization process, have been mostly identified in Medicago truncatula and Lotus japonicus, as well as in rice, according to Pimprikar and Gutjahr, 2018 and to Lanfranco et al., 2018. The scheme is modified from Bonfante and Genre, 2010.

some short ribosomal sequences. Trying to put order in this for Mucoromycota (Gray et al., 1986), six years later than the still magmatic scenario, Desiro et al. (2017) carefully investi- Saccharomyces cerevisiae TRP1 gene (Tschumper and Carbon, gated the so far available sequences of Endogonales and - per- 1980). The advent of the genomic era represented a complete forming a multigene phylogeny - detected two deeply turnaround towards explorative and descriptive research, divergent clades, delimited as two new families, Endogona- and offered a chance to enlighten fungal biology from a ceae and Densosporaceae. While the latter consists of the different perspective. The first whole genome sequence for a genera Densospora, Sphaerocreas, and many diverse lineages Mucoromycota has been deposited in 2005 (two years after known only from environmental DNA sequences of plant- than the leading work on Neurospora crassa by Galagan et al., endocellular fungi, Endogonaceae includes species as Endo- 2003), and published in 2009 (Ma et al., 2009): it’s not surprising gone and Jimgerdemannia with an ectomycorrhizal habitus. that the fungal candidate was Rhizopus delemar (formerly The emerging data seem therefore to suggest that Mucoro- Rhizopus oryzae), due to the threat this fungus represents for mycotina harbour significant undescribed diversity and are a human health as an agent of mucormycosis. Among the key relevant source of plant-interacting fungi. The capacity to discoveries were the abundance of TEs (20%, twice as many colonize plant tissues and to produce arbuscules seems to as N. crassa), the presence of a whole genome duplication be present in both Mucoromycotina and Glomeromycotina, associated with drug resistance, and the characterization of while the ectomycorrhizal traits are shared with many other developmental genes representing a potential target for ther- fungal taxa from Basidio- and Ascomycota (Tedersoo and apeutic purpose. Currently, 80 Mucoromycota genomes are Smith, 2013). available at JGI mycocosm (https://mycocosm.jgi.doe.gov/ mycocosm/home), with Mucoromycotina being the mostly covered sub-phylum (59 genomes), followed by Mortierello- 3. Genome sequencing of Mucoromycota: a mycotina (111 genomes) and by Glomeromycotina (10 ge- focus on Glomeromycotina nomes). Most of the sequenced genomes belong to saprotrophs such as Rhizopus, Mucor, Phycomyces, and Mortier- Starting from the eighties, the journey through genomic DNA ella, while a limited number of plant symbionts have been (gDNA) sequencing, seemed to be slightly delayed for Mucoro- sequenced from the genera Jimgerdemannia, Endogone (Mucor- mycota, when compared to other fungal groups. According to omycotina; Chang et al., 2019), and from the sub-phylum the NCBI records, an aspartyl protease from Mucor miehei was Glomeromycotina, starting from Rhizophagus irregularis the first gDNA sequence generated with the Sanger technique

Please cite this article as: Bonfante, P., Venice, F., Mucoromycota: going to the roots of plant-interacting fungi, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.003 The roots of plant-interacting fungi 5

(Tisserant et al. 2013; Lin et al., 2014). At the same platform, same way for fungi in general. This last analysis partially 778 and 457 genomes are currently available for Ascomycota confirmed previous results, with words such as “mucormyco- and Basidiomycota, respectively. This probably reflects the sis”, “catalytic” and “hydrolase” but, at the very core of the difference in the abundances of identified species between resulting wordcloud, we found terms that highlight the capac- Mucoromycota and Dikarya, but also highlights a particular ity of Mucoromycota of associating with plants, such as research focus on Mucoromycota, which contains human “roots”, “symbiosis” and “stable”. Even if Mortierellomycotina pathogens, producers of molecules of human interest, post- and Mucoromycotina contain fungi that associate with plants, harvest disease agents and fermenters (Gryganskyi et al., the results are essentially driven by AM fungi, as demon- 2018), in addition to symbionts. strated by the presence of the term “amf”, which is the most What does DNA research in Mucoromycota talk about? To frequent in the plot. answer this question, we performed a text mining analysis Due to their capacity to establish mutualistic symbiosis where we considered 160 abstracts associated with Mucoro- with most land plants, AM fungi are essential members of eco- mycota GenBank records from the last five years, and clus- systems, where they “transport” (“symbiosis” topic in Fig. 3a) tered words into main topics (Fig. 3a; Supplementary Fig. 1). inorganic nutrients (mostly inorganic phosphate) from the Two of these topics contained words associated with patho- soil to their plant hosts. Studies on their potential application genesis and potential industrial applications. In addition, as enhancers of plant fitness and productivity in agricultural two other topics seemed to point out at fungal-plant symbiotic systems, which already flourished in the pre-genomic era associations, and to the importance of Mucoromycota as de- (Azcon-Aguilar and Barea, 1997; Sharma et al., 1997), will prob- graders in ecosystems. To confirm that these issues are partic- ably live a new life in the light of the recent genomic data ularly important for Mucoromycota, we performed a (Chen et al., 2018; Posta and Duc, 2019). Despite the interest differential word abundance analysis (Fig. 3b), i.e. compared raised by their biology, the first genomic sequence from AM the same abstracts, with a reference set obtained in the fungi was the mitochondrial genome of Rhizophagus irregularis

Fig. 3 e Results of a text mining analysis performed to highlight the main topics in Mucoromycota genome research. All the analyses were performed in R environment by using the “quanteda” and topicmodels packages (Benoit et al., 2018; Grun€ and Hornik, 2011). The statistical analyses have been performed on a set of 167 abstracts, as obtained by querying the Pubmed database with the word “Mucoromycota”. The search has been restricted to articles published within the last 5 years. a) By considering each abstract related to Mucoromycota as a separate document, the topicmodels package was used to predict statistical groups, or “topics”, where words were clustered based on their co-occurrence throughout the analyzed docu- ments. The names for each topic were assigned manually. For each box, the frequency of the most relevant words associ- ated with a topic is shown. Words are truncated due to the “stemming” process, which computationally reduces words to their most meaningful portion. b) The same abstracts used for the topic prediction analysis (target set) was compared with a reference set, obtained with the same procedure, and made of the same number of randomly picked abstracts associated with fungi in general. The size of each word in the resulting wordcloud is the chi-squared value calculated comparing the frequency of the word in “target” vs “reference” (and vice versa). Thus, the larger the word size, the more target- or reference- specific is the word.

Please cite this article as: Bonfante, P., Venice, F., Mucoromycota: going to the roots of plant-interacting fungi, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.003 6 P. Bonfante, F. Venice

(Lee and Young, 2009), while the nuclear genome of the same homology-basis (Morin et al., 2019; Zeng et al., 2018), but fungus, which became a model species, was published only in they probably guarantee a robust communication between 2013 and 2014, with two studies that targeted a group of sepa- AM fungi and their hosts. What also joins the genomes of rate nuclei as well as individuals (Lin et al., 2014; Tisserant AM fungi and other obligate biotrophs is the absence/limited et al., 2013). This delay can be explained while looking at the presence of plant cell wall degrading enzymes, a trait that aspects which were traditionally associated to the biology of may be involved in eluding host defense and maintaining AM fungi: they were described as asexual, obligate biotrophs, the viability of host cells. In the case of AM fungi, this is essen- that cannot be reproduced axenically or be genetically trans- tial to maintain the flux of photosynthetic byproducts from formed, and have aseptate hyphae where hundreds of nuclei the plant to the fungus, as both genomic data (Kobayashi co-exist within a single cytoplasmic stream. While genomics et al., 2018) and plant mutants (Bravo et al., 2017; Luginbuehl changed some of our views on sexuality and obligate bio- et al., 2017), revealed a full dependence of AM fungi on trophism in AM fungi (see below), the first sequences of R. plant-derived lipids. Their genomes lack a cytosolic Fatty irregularis genome highlighted another key feature represent- Acid Synthase complex that is common to fungi (FASI), but ing a technical challenge: its genome was the largest by far an- possess a mitochondrial FASII for the synthesis of lipoic acid notated for fungi (140 Mbp, Table 1), and the gene number (Dearth et al., 2018; Kobayashi et al., 2018). This feature, ranged from 27000 to 28000 (twice as many as in R. delemar). together with the apparent lack of a genetic machinery sup- More recent projects confirmed this characteristic for other porting the biosynthesis of thiamine and the limited uptake AM fungi (Kobayashi et al., 2018; Morin et al., 2019; Sun of sugars from soil (Tisserant et al., 2013), contributes on one et al., 2019): AMF genomes are among the largest in the fungal hand to the signature of AMF as obligate biotrophs; on the kingdom, ranging from 125 Mbp for the A1 strain of R. irregula- other hand, genomics investigations offer solutions to unlock ris to the striking sizes of 570 Mbp of Gigaspora rosea (Morin the enigmatic lifestyle of AM fungi. Starting from this current et al., 2019) and 770 Mbp of G. margarita (Venice et al., 2019). knowledge, novel studies demonstrate that R. irregularis can In these two species, the gene number is comparable with Rhi- be grown and reproduced axenically on a medium added zophagus and Diversispora epigaea (Sun et al., 2019), but the with fatty acids, among which myristate (Kameoka et al., genome size was inflated by a huge amount of TEs, which 2019; Sugiura et al., 2019). An enriched gene catalogue deputed occupy around 70% of their genomes. This value makes these to phosphate transport (Venice et al., 2019; “symbiosis” topic species similar to ectomycorrhizal Pezizomycotina (Table 1) in Fig. 3a) and the presence of genes of primary metabolism and to obligate biotrophic pathogens such as the powdery horizontally transferred from plants (Li et al., 2018) demon- mildew Blumeria graminis (Spanu et al., 2010), also suggesting strate the long history of this fungal-plant interaction. While an association between TEs invasion and obligate plant bio- all AM genomics studies agreed on their obligate biotrophy, trophic lifestyle. Similar to these species, AM genomes encode the amount of variation between nuclei in single AM species for a large number of effectors (Table 1): these proteins are still was strongly debated. The increased availability of single nu- uncharacterized and identified uniquely on sequence cleus sequencing techniques allowed to clarify this point: an

Table 1 e Summary statistics for the fungal genomes commented throughout the text. Whether the TEs proportion of one fungal genome was not commented in the related publication, it was calculated with Linux bash scripts starting from the masked genome assemblies found on the JGI Mycocosm website (https://mycocosm.jgi.doe.gov/mycocosm/home). Species and strains Genome size N. of contigs/ Repeats Number Number of Reference (Mbp) scaffolds genome of genes putative small coverage (%) secreted effectors

Rhizophagus irregularis A1 125.86 11,301 22.69 26,659 293 Chen et al. (2018) Rhizophagus irregularis DAOM197198 136.08 1,123 26.38 26,183 366 Chen et al. (2018) Rhizophagus erebriforme DAOM 227022 136.89 2,592 24.77 21,158 252 Morin et al. (2019) Rhizophagus diaphanus MUCL43196 125.87 2,764 20.18 23,252 291 Morin et al. (2019) Diversispora epigaea IT104 156.58 731 43.6 28,348 w400 Sun et al. (2019) Gigaspora rosea DAOM194757 597.95 7,526 63.44 31,291 601 Morin et al. (2019) Gigaspora margarita BEG34 773.1 6,490 64 26,603 548 Venice et al. (2019) Endogone sp. FLAS F-59071 96 15,409 65.6 9569 222 Cheng et al. (2019) Jimgerdemannia flammicorona AD002 231 35,354 77.6 13,838 316 Cheng et al. (2019) Jimgerdemannia flammicorona GMNB39 240 33,875 78.1 13,653 299 Cheng et al. (2019) Jimgerdemannia lactiflua OSC 612217 180 45,525 72.9 12,651 280 Cheng et al. (2019) Mortierella elongata AG77 49.63 473 4.63 14,969 Unknown Uehling et al. (2017) Mortierella alpina ATCC#32222 38.38 476 1.76 12,796 Unknown Wang et al. (2011) Rhizopus delemar 99-880 45.3 389 19.64 17,467 Unknown Ma et al. (2009) Rhizopus microsporus ATCC52813 25.97 131 4.65 10,905 Unknown Mondo et al. (2017) Tuber melanosporum Mel28 124.95 398 57.73 10,058 125 Martin et al. (2010) Laccaria bicolor S238NeH82 60.71 55 41.5 23,132 278 Martin et al. (2008) Blumeria graminis f. sp. hordei DH14 118.73 6,843 63.7 6,470 248 Spanu et al. (2010) Phycomyces blakesleeanus NRRL1555 53.9 80 9.74 16,528 Unknown Corrochano et al. (2016)

Please cite this article as: Bonfante, P., Venice, F., Mucoromycota: going to the roots of plant-interacting fungi, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.003 The roots of plant-interacting fungi 7

in-depth analysis of MAT-loci, which are related to cryptic et al., 2019), seems to be the only AM species encoding for a sexuality events in AM fungi (Riley et al., 2014), revealed that putative cryptochrome. some strains of R. irregularis are heterokaryotic, and that In conclusion, Mucoromycota genomic data can be mined extensive recombination among nuclei can be observed at following two directions: are the roots of the symbiotic life these loci (Chen et al., 2018; Mathieu et al., 2018). Furthermore, style, iconic of Glomeromycotina, detectable in Mucoromyco- the availability of multiple sequenced strains from the same tina and Mortierellomycotina? and on the other hand is the species, revealed an impressive amount of intra-specific vari- perception of chemical-physical stimula allowed by AM ge- ability (the R. irregularis strains only share around 8000 nomes? A quick look at their still largely undescribed genomes conserved genes), such that the concept of “pangenomes” reveals an undiscovered richness: more studies can flourish to has been suggested to describe AM genomes (Mathieu et al., shed light on these odd fungi. 2018). All these features remained among the main targets for genomics in AM fungi, as highlighted in Fig. 3bwhere,for example, words such as “fatty” and “sex” resulted as very 4. Endobacteria: a common trait of frequent. What will be the contribution of genomics in Mucoromycota studies regarding AM fungi and, more in general, Mucoromy- cota?Plantsandsymbiosisseemtobetheleastcommonde- In 1996, Bianciotto and colleagues reported that the obligate nominator for these basal fungi, that are yet so diverse. endosymbiotic mycorrhizal fungus G. margarita harbors Besides AM fungi, Mortierella speciesarefoundasrootendo- Gram-negative intracellular bacteria (Bianciotto et al., 1996), phytes, and their communities are shaped by plant phospho- which are Burkholderia-related. In 2005, Partida-Martinez and rous content (Bodenhausen et al., 2018), while members of Hertweck discovered that the pathogenic R. microsporus Endogonales (Mucoromycotina) can be both ectomycorrhizal harbored endosymbiotic bacteria, which turned out to be and endophytes of basal plants (Chang et al., 2019), demon- responsible for toxin production (Partida-Martinez and strating that the symbiotic potential of these fungi crosses Hertweck, 2005). In 2015, Desiro and colleagues found that Jim- the whole plant kingdom (Fig. 1). Genomic data could help gerdemannia lactiflua hosted Mycoplasma-related endobacteria the identification of a putative symbiotic machinery in com- (Desiro et al., 2015), which had already been detected under mon to all Mucoromycota. Tracing back to the common the electron microscope by Bonfante and Scannerini (1977). ancestor of Mucoromycota may also involve fatty acid meta- Lastly, when sequencing the genome of M. elongata, Uehling bolism: despite the absence of FASI in Glomeromycotina, a and colleagues (2017) also assembled a bacterial genome, rich toolkit for the elongation and modification of fatty acids which had previously been detected by Sato et al. (2010) and is present in Mucoromycota, from oleaginous fungi such as later named Mycoavidus cysteinexigens (Ohshima et al., 2016). M. elongata (Uehling et al., 2017)toR. irregularis (Wewer From an evolutionary point of view, it is exciting to see that et al., 2014). all the fungi in which these endobacteria have been consis- Parallel to this topic, AM genomes need to be deeply tently detected belong to the three Mucoromycota subphyla. investigated in the light of their idiosyncrasies: since now, By contrast, Burkholderia- and Mycoplasma-related endobacte- the impact of TEs, genomic erosion and genetic drift in ria have never been found in Ascomycota or Basidiomycota, shaping the evolution of AM fungi have been evaluated where endobacteria with free-living capacities have been only in some isolates. AM fungi, as other mycetes, may be often observed (Arendt et al., 2016.; Guo et al., 2017). All of subjected to these dynamics due to their asexual and obli- the Mucoromycotaebacterial interactions have been deemed gate nature (Menardo et al., 2017; Spanu, 2012), even if these ancient and some of them dated back to the Devonian traits can be weakened by data on their hidden sexuality and (Mondo et al., 2012). The findings have led to the hypothesis potential capacity to grow in the absence of the host, as that the ancestors of Mucoromycota already hosted endobac- described before. VanKuren and colleagues (2013) demon- teria in their cytoplasm before the speciation events that led strated that while asexual, Claroideoglomus etunicatum is to the taxon diversification (Bonfante and Desiro, 2017). capable of purging deleterious mutations and therefore is To date, two endobacterial groups have been found, the not likely of experiencing high genetic drift/genome erosion. rod-shaped Betaproteobacteria (Burkholderia-related endo- Finally, as a novel topic, genomics could offer a platform to symbionts [BREs]) and coccoid Mollicutes (Mycoplasma-related uncover poorly investigated features. For example, very little endosymbionts [MREs]). The BRE B. rhizoxinica produces the is known about the reaction of AM fungi to physical and abovementioned rhizoxin used as a virulence factor by its chemical stimuli, which could be relevant to their biotechno- host R. microsporus (Partida-Martinez and Hertweck, 2005) logical application (El-Esawi, 2018) and is already largely and also affects fungal reproduction (Mondo et al., 2017; acknowledged for Mucoromycota in general (Corrochano Partida-Martinez et al., 2007); M. cysteinexigens has been et al., 2016). To highlight the unexplored richness of AM ge- detected in many taxa of Mortierellales (Takashima et al., nomes, we searched the AM genomes for genes related to 2018) as well as Candidatus Glomeribacter gigasporarum light perception and circadian rhythm regulation (Fig. 4). Be- (CaGg), thriving in Gigasporaceae (Pawlowska et al., 2018). sides being mainly hypogeous fungi, we found that they MREs, with their coccoid shape, have been detected in many possess genetic determinants that vary across the genera AM fungi as well as in G. pyriforme (Naumann et al., 2010), in and are putatively involved in the perception of the light Endogonales (Desiro et al., 2015) and some Mortierellales stimulus and circadian rhythm regulation; specifically, Diver- strains (Desiro et al., 2018). Their multiple and sometimes sispora epigaea, which produces epigeous fruiting bodies (Sun simultaneous presence (Desiro et al., 2015, 2018) opens

Please cite this article as: Bonfante, P., Venice, F., Mucoromycota: going to the roots of plant-interacting fungi, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.003 8 P. Bonfante, F. Venice

Fig. 4 e Genes associated with light perception and circadian rhythm in AMF. a) The plot shows, for each species, presence/ absence of homologs of the Neurospora crassa genes involved in light perception and circadian rhythm regulation (Chen and Loros, 2009). The homologs were searched as follows: for each N. crassa gene, a list of fungal homologs has been downloaded from the NCBI protein database. The proteins obtained this way were aligned with Clustal Omega v1.2.4 (Sievers and Higgins, 2014) and an HMM model was built to be used as a query with HMMER v3.1.2 (Eddy, 2011). The search was per- formed against the AMF proteomes separately, and hits with an Evalue>10e-50 were discarded. Two putative copies of white collar 2 are present in the proteomes of the Rhizophagus species; however, for sake of simplicity, the scheme only shows the presence of the one with the lowest Evalue (as the putative copies were found with an Evalue between 10e-50 and 10e-100). b) A simplified representation of the putative role of the genes found in a), based on their homologs in N. crassa and other fungi (Yu and Fischer, 2019). The white collar 1 - white collar 2 (wc1-wc2) complex is thought to function as both a receptor (wc1) and a transcriptional regulator (wc2); its assemblage in presence of the light stimulus leads to the positive transcrip- tional regulation of a variety of developmental processes, and also promotes the transcription of frequency clock protein (FRQ). FRQ functions in a negative feedback loop where it inhibits the function of the wc1-wc2; since its accumulation is gradual during the day, FRQ is fundamental in regulating the biological processes associated with lightedark transitions. By contrast, besides the fact that they can perceive light, little is known on the way cryptochrome (CRY) and the seven- transmembrane rhodopsin-like receptors regulate biological processes in fungi.

many questions about who arrived first and about their func- they have adopted a nonlethal parasitic lifestyle, at least in tional roles. Mortierellomycotina (Desiro et al., 2018). The genome sequencing of many of these bacterial isolates By contrast, the impact of BREs has been more carefully has allowed us to identify some common features in the BREs investigated; the availability of a cured line of G. margarita (Bonfante et al., 2019). When compared to Burkholderia, which revealed finely tuned benefits provided by CaGg. It positively represents the common-reference free-living bacteria, they influences fungal presymbiotic growth and influences the possess reduced genomes ranging from 3.7 to 1.8 Mbp, even fungal phenotype (increasing lipid storage and controlling if some of these genomes are incomplete and could be larger cell wall thickness). Detailed omics and biochemical analyses when closed. They all have lost some biosynthetic capabilities revealed that CaGg has a strong impact on the transcriptomic related to primary metabolism and to specialization in fungal profile of G. margarita, leading to profound changes in mito- metabolite uptake. B. rhizoxinica uses host-derived lipids for chondrial metabolism that range from higher ATP production, energy (Lastovetsky et al., 2016), while M. cysteinexigens to the regulation of calcium flow, to more efficient responses (Uehling et al., 2017) and CaGg (Ghignone et al., 2012) import to oxidative stress and increases in glutathione metabolites fungal amino acids and use fungal organic acids for energy. (Dearth et al., 2018; Salvioli et al., 2016; Venice et al., 2017). Lastly, these BREs have retained secondary metabolite gene All of these emerging results suggest that Mucoromycota, clusters and multiple secretion systems (from Type II to Types thanks to their aseptate mycelium, may act as efficient vec- III and IV). MREs have high genetic variability and a strongly tors for endobacteria, which therefore represent the intracel- reduced genome of 0.6e1.3 Mbp. MREs from Endogone and Jim- lular microbiota (Desiroetal.,2014 ) of these early-diverging gerdemannia flammicorona (Chang et al., 2019), Dentiscutata het- fungi (Bonfante et al., 2019). They also reveal that these erogama (Torres-Cortes et al., 2015), Racocetra verrucosa (Naito endobacteria are mostly vertically transmitted and are et al., 2015), and Diversispora epigea (Sun et al., 2019) have strictly dependent on their hosts, whereas the fungal hosts been sequenced, but their genomes remain quite enigmatic can proliferate in their absence. Indeed, some Mortierella and poorly deciphered. Moreover, their impact on their fungal strains produce more biomass when cured (Uehling et al., hosts is still unclear, although a current hypothesis is that 2017; Desiroetal.,2018 ). However, in an evolutionary context

Please cite this article as: Bonfante, P., Venice, F., Mucoromycota: going to the roots of plant-interacting fungi, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.003 The roots of plant-interacting fungi 9

and under natural conditions, we suggest that endobacteria the two endophytes, which at cellular level are very similar. act as genetic factors that increase the variability of their On the basis of the strikingly different phenotypes (coils vs. fungal hosts. Natural selection may therefore operate, acting arbuscules), we could hypothesize that Mucoromycotina sup- on individual fungal isolates that also differ for the presence porting colonization in non-seed plants are diverse from those or absence of endobacteria. We suggest that probably these present in Medicago truncatula, where thin arbuscules are pro- microbes living inside the fungal cytoplasm offer benefits duced (Orchard et al., 2017). Liverworts accommodate AM under natural conditions that have not yet been fully fungi, which produce the typical arbuscules (Ligrone et al., identified. 2007), demonstrating that also haploid, non-seed plants may support arbuscule development. Endogonales has been evalu- ated as originating in the mid to late Silurian (w420 Ma), 5. How many still opened questions for Plant- contemporaneous with the origin of Glomeromycotina interacting Mucoromycota? (Chang et al., 2019), suggesting that both groups were present during the early events of land plant colonization. However, Omics approaches have certainly contributed to the under- the phylogenomic analyses were based on Endogonales with standing of Mucoromycota biology and of their multiple inter- saprobic (Endogone) or ectomycorrhizal (Jimgerdemannia) actions with plants, starting from the phylogenomics analysis habitus (Chang et al., 2019), leaving the relationships between (Spatafora et al., 2016) which has solved many idiosyncrasies Densosporaceae and Glomeromycotina unresolved. A further related to this heterogeneous fungal group. However, coming question is whether the Endogonales are easily grown in pure back to the first hypothesis (were Mucoromycota the first culture or whether they are obligate, plant-dependent symbi- group of fungi that interacted with plants?) we have to admit onts such as their Glomeromycotina relatives. that the answer is not clear-cut. Fossil reports are sometimes Another unsolved point is the presence of G. pyriforme at ambiguous: indeed, although the highly branched arbuscules the base of the Glomeromycotina. This unusual fungus, which produced by the Glomeromycotina seem to be convincingly lives without interacting with plants but is dependent on the recognizable in fossil matrices, simple hyphae or swollen presence of Nostoc colonies (http://www.geosiphon.de/geosi- structures may belong to multiple organisms. The absence phon_home.html), has a free-living stage, since Nostoc enters of fossil reports for liverworts and the discovery that today the fungus by horizontal transmission. This means that, at the model liverwort Marchantia can be colonized by the oomy- least in theory, G. pyriforme could have a saprobic phase, cete pathogen Phytophthora palmivora (Carella et al., 2018) lead- even if it is not clear how long this phase is. Could AM fungi ing to fungal-like intracellular structures, raise a new arise as saprobes? Did they lose this capacity by losing their question: can pathogenic and beneficial interactions be reli- lipid biosynthetic pathway? Lipid metabolism is a specific ably recognized on the basis of fossil descriptions? Indeed, aspect of the symbiosis between R. microsporus and its endo- molecular clock estimates place the origin of oomycetes as symbiont B. rhizoxinica: Lastovetsky et al. (2016) demonstrated occurring by at least the mid-Paleozoic (w430e400 Ma) that adjustments in fungal lipid metabolism mediated by (Matari and Blair, 2014), which is the origin timing hypothe- diacylglycerol kinase are required for the mutualistic outcome sized for other Mucoromycotina, such as Endogonales of the Rhizopus-Burkholderia symbiosis. Along the same lines, (Chang et al., 2019). endosymbiont-bearing G. margarita and its cured line reveal The second crucial unsolved question concerns Mucoro- a different lipid profile (Salvioli et al., 2010), confirming that mycotina and the order Endogonales, which is surely a novel lipid metabolism is crucial in plant-fungal-bacterial networks. source of plant-interacting fungi (Hoysted et al., 2018). Howev- Investigating the G. pyriforme genome could provide some er, it seems that crucial information is still missing: evidence hints about the properties of AM fungi. of the capacity of this group to support ectomycorrhizal for- Although some of the questions raised here can be mation is based mostly on molecular data, with only limited resolved in the future in a straightforward fashion, for morphological characterization (Yamamoto et al., 2017 and example through the sequencing of basal Glomeromycotina Desiro et al. 2017 for a review of previous findings). It would and/or other Endogonales, others will require new ap- be interesting to know whether the peculiar phenotype proaches. The new field of synthetic biology and experi- described by Fassi et al. (1969) and Bonfante and Scannerini mental evolution of symbiosis have already allowed (1977)di.e., reduced mantel and Hartig net with some intra- researchers to demonstrate that the transfer of the sym cellular colonizationdcan be confirmed under laboratory plasmid to a Ralstonia strain may transform the pathogen conditions. into a symbiotic N-fixing bacterium over generations In regard to the capacity of Densosporaceae to support endo- (Clerissi et al., 2018) and to demonstrate that a saprobic Mor- mycorrhizae, there remain grey areas in the current informa- tierella strain can live associated to a photosynthetic organ- tion: the strain used by Field et al. (2015) was directly isolated ism (Du et al., 2019). These new approaches could shed new from a Treubia thallus and showed a colonization pattern with light on the fascinating issue of the origin and evolution of coils and lumps, whereas the small arbuscules produced by plant-interacting fungi. the so-called G. tenuis (Orchard et al., 2017) seem to be pro- duced by a fungus whose short sequences also cluster in the Densosporaceae clade (Desiro et al., 2017, Walker et al., Glossary 2018). The simultaneous detection of Glomeromycotina and Mucoromycotina (Rimington et al., 2015) surely requires Mycorrhizal symbiosis: the symbiotic association established further approaches, such as in situ hybridization, to identify between soil fungi and the 90% of land plants, in which plant

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reduced carbon is exchanged for mineral resources acquired Bonfante, P., 2018. The future has roots in the past: the ideas and by the fungi from the soil. scientists that shaped mycorrhizal research. New Phytol. 220, e Ectomycorrhiza: identifies the mycorrhiza present in the 982 995. https://doi.org/10.1111/nph.15397. roots of many Gymnosperm and Angiosperm trees; it in- Bonfante, P., Desiro, A., 2017. Who lives in a fungus? The diver- sity, origins and functions of fungal endobacteria living in volves both Asco- and Basidiomycota, as well as Mucoromycota. ISME J. 11, 1727e1735. https: Mucoromycotina. //doi.org/10.1038/ismej.2017.21. Arbuscular mycorrhiza: the more common type of mycor- Bonfante, P., Scannerini, S., 1977. Cytological observations on the rhizal symbiosis established between Glomeromycotina and mycorrhiza Endogone flammicorona-Pinus strobus. Allionia 22, around 72% of land plants; its name originates from the 23e34. typical fungal structures, the arbuscules. Bonfante, P., Venice, F., Lanfranco, L., 2019. The mycobiota: fungi Phylogenomics: the analyses that involve genome data take their place between plants and bacteria. Curr. Opin. Mi- crobiol. 49, 18e25. and evolutionary reconstructions, linking the fields of geno- Bravo, A., Brands, M., Wewer, V., Dormann,€ P., Harrison, M.J., mics and evolution. 2017. Arbuscular mycorrhiza-specific enzymes FatM and Endobacteria: bacteria which live inside the cytoplasm of RAM2 fine-tune lipid biosynthesis to promote development of Eukaryotes, such as Insects or Fungi. arbuscular mycorrhiza. New Phytol. 214, 1631e1645. https: //doi.org/10.1111/nph.14533. Carella, P., Gogleva, A., Tomaselli, M., Alfs, C., Schornack, S., 2018. Declaration of Competing Interest Phytophthora palmivora establishes tissue-specific intracel- lular infection structures in the earliest divergent land plant The authors have no conflict of interest to declare. lineage. Proc. Natl. Acad. Sci. 115, E3846eE3855. https: //doi.org/10.1073/pnas.1717900115. Chang, Y., Desiro, A., Na, H., Sandor, L., Lipzen, A., Clum, A., Barry, K., Grigoriev, I.V., Martin, F.M., Stajich, J.E., Smith, M.E., Acknowledgements Bonito, G., Spatafora, J.W., 2019. Phylogenomics of Endogona- ceae and evolution of mycorrhizas within Mucoromycota. Research was funded by local grants (60%) to Dr. Paola Bon- New Phytol. 222, 511e525. https://doi.org/10.1111/nph.15613. fante. The authors are grateful to Dr Alessandro Desiro and Chen, E.C., Mathieu, S., Hoffrichter, A., Sedzielewska-Toro, K., Peart, M., Pelin, A., Ndikumana, S., Ropars, J., Dreissig, S., Dr J. Mach for the critical reading of the manuscript as well Fuchs, J., Brachmann, A., Corradi, N., 2018. Single nucleus as to the two anonymous referees for their careful and expert sequencing reveals evidence of inter-nucleus recombination comments. in arbuscular mycorrhizal fungi. eLife 7e39813. https: //doi.org/10.7554/eLife.39813. 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