Abstract
Most land plant species have their roots colonized by arbuscular mycorrhizal fungi (AMF). These symbiotic associations are often found in the roots of field crops. The biological basis and practical significance of this symbiosis have been extensively studied, and the molecular mechanisms underlying the initial colonization process and the nutrient exchange between the host plant and the AMF have been elucidated. However, developmental processes and turnover of elements of the mycorrhiza, and the resulting changes in mycorrhizal function, are not well understood. The enigmatic nature of the development-function relationship is probably due to the short life span of the infection unit, which has largely been overlooked in studies investigating mycorrhizal function at the macroscopic level. This paper outlines the concept of the infection unit and functional expression patterns in terms of the transient aspects of the micro-symbiont during its life cycle in this symbiosis.
Keywords
- arbuscular mycorrhiza
- functional molecular markers
- infection unit
- life cycle
- live imaging
1. Introduction
The roots of approximately 95% of vascular land plant species, with the exception of some families (e.g., the Brassicaceae, Amaranthaceae, and Polygonaceae), are colonized by symbiotic fungi which form a mutualistic relationship (mycorrhiza) with the host plant roots [1, 2]. Approximately 10% of vascular plant species, mostly woody species, are colonized by ectomycorrhizal fungi, which belong to the
AMF can also colonize thalli of the early nonvascular land plants, namely, the liverworts and hornworts [13, 14]. Phylogenetic analyses indicated that symbiotic genes are present in the genomes of these early land plants, with the functions of the encoded proteins being conserved, suggesting that this symbiosis is phylogenetically widespread in plants [15]. AM symbiosis is beneficial for plants in relation not only to nutrition but also to the mitigation of biotic and abiotic stresses (e.g., resistance to pathogens, tolerance of drought and toxic element stress, increased biomass production, and secondary metabolite accumulation) [16, 17, 18, 19]. Hence, the functionality of AM symbiosis can influence the productivity and quality of crops.
The effects on the host plant of AM symbiosis are commonly investigated by inoculation of the roots of the host plant with a (usually) single-species AMF in pot culture. However, field-grown inoculated roots can harbor AMF species other than the test AMF species, the functionality of which would not have been tested using an inoculation test because not all AMF in the roots can sporulate [20]. In addition, not all AMF which colonize roots are active and functional [21, 22], and the colonization process and the stability of the colonization by diverse AMF species in the same field-grown roots are unclear [23]. Overall, under field conditions, the functionality of AM symbiosis is probably based on unknown but highly dynamic associations between plants and a diverse range of AMF species. To better understand this complex association, in the current article, the colonization dynamics of AMF species in roots will be discussed. To understand the functional unit of the plant-AMF symbiosis, it is important to outline the concept of the colonization unit.
2. Latent colonization dynamics in arbuscular mycorrhizas
In 1905, an illustration by Gallaud showed that root cortical cells often contain “clumps” of arbuscules (Figure 1) [24]. Subsequent morphological examination of mycorrhizal roots at the cellular level suggested that this intracellular colonization may be ephemeral [25, 26, 27]. Following this, morphometric studies, coupled with electron microscopy, calculated that the life span of an intact arbuscule in several plant species was a minimum of 2.5 days [28, 29]. Such a limited life span of the units of intracellular colonization by AMF can be generalized because these arbuscule clumps have been observed in many plant species, including the relatively primitive nonvascular plant, the liverwort [13]. Why does this mutually beneficial association exhibit such short-lived units of intracellular colonization? Unfortunately, our understanding of this phenomenon has not increased much since the first observation of arbuscule clumps by Gallaud more than 110 years ago.
Advances in the forward and reverse genetic approaches available to decipher the molecular mechanism for the AMF colonization process have shown that several signaling mutants of model plants exhibited compromised AMF epidermal penetration and altered chemical and cellular crosstalk in the initial stages between plants and AMF [10, 30]. Recently, several mutant lines exhibited suppressed intraradical colonization, forming prematurely senescent or stunted arbuscules [11, 31]. Some plant genes have been implicated in the cellular process of arbuscule degeneration [32, 33, 34, 35]. The degeneration process of arbuscules has also been shown to be related to colonization level, illustrating the importance of arbuscule life cycle to the development of mycorrhiza. In addition, live imaging of the green fluorescent protein (GFP)—symbiotic phosphate transporter (PT11) fusion protein in the roots of mycorrhized rice seedlings—also revealed the limited life span of the units of intracellular colonization, in which the rapid collapse of arbuscules was observed [36]. The mechanism of mycorrhization, coupled with such a short life span of the individual colonization unit, has been addressed by continuous (long-term) live imaging of the symbiotic marker secretory carrier membrane protein (SCAMP) [37], where successive de novo colonizations underlie AM development (SubSection 2.2). These findings emphasize the importance of the life cycle of colonization when we consider the dynamics of AM functionality.
2.1 Concept of the infection unit
In soils, there are many different AMF species, and no strict host-AMF specificity has been observed [38, 39]. Accordingly, under field conditions, co-colonization of the same root by multiple AMF species can occur [2]. It is likely that the functionality of these diverse AMFs is not the same, and colonization by each AMF may last only a short time. Therefore, to correctly characterize the functionality of field mycorrhizas, the colonization process, the dynamics, and the functionality of the diverse AMFs in the roots need to be understood.
When the fungal spore germ tubes approach the root surface, chemical crosstalk occurs between the roots and the AMF hyphae, triggering the molecular and cellular remodeling process necessary for hyphal entry into the roots [11]. Coinciding with this pre-symbiotic crosstalk, AMF hyphae around the roots are often highly branched, giving rise to a characteristic cascade-like mycelium, composed of lateral branches [2]. Several plant mutants exhibiting disruption of the early signaling process fail to allow hyphal penetration of the epidermal layer [10, 11], suggesting the importance of this initial mutual recognition process.
After hyphopodia are formed, hyphae penetrate the rhizodermal layer and grow longitudinally in the root cortex. Short branches from the longitudinally extending hyphae penetrate the cortical cell walls and branch dichotomously in the cell lumen to give rise to arbuscules. Importantly, the maximum elongation in the cortex of hyphal structures derived from a single or a few hyphal penetrations of the epidermis are reported to be up to 20 mm [2]. In rice seedlings, however, the maximum elongation in the cortex of hyphal structures derived from the entry point is only 0.5 mm [37]. In general, the area occupied by each colonization unit derived from a single epidermal entry is difficult to recognize, because intraradical hyphae derived from different entry points immediately overlap one another to form a larger colonization area within the cortex. The rates of growth of intraradical colonization are reported to range from 0.13 to 1.22 mm/day [2]. In the live imaging of mycorrhizal rice roots, the rate varied from 0.42 to 1.68 mm/day [36]. Although the maximum length of intraradical colonization derived from one or a few penetrations varied greatly among studies, these independent colonies of mycelia are called the “infection unit” (Figure 2) [25].
2.2 Development and functionality of mycorrhizas: an infection unit-based view
The development of the mycorrhiza and the dynamics of the infection unit are tightly linked processes during mycorrhization. It is also likely that the functionality of mycorrhiza in the field is also variable, depending on the functionality of the infection unit that is derived from different AMF species. Live in situ imaging revealed that multiple infection units overlap to form a larger infection (“colonized region”) within a few days [36, 37, 40], making the delimitation of each infection unit experimentally difficult. Coupled with the difficulty of differentiating between different AMF species in the roots, using morphological or molecular approaches [41, 42], the dynamic process of mycorrhization has probably hampered progress in characterizing the infection unit-based functionality of field mycorrhizas. Live imaging of rice mycorrhizal roots revealed that the expansion of the colonized region occurs in concert with successive de novo formation of multiple infection units (Figure 2) [37].
However, a better understanding of the dynamics of the mycorrhization process depends substantially on the quality and the ease of imaging of the hyphae within the roots. Traditionally, cytological studies of the colonization process have been performed with chemical staining of fixed (i.e., dead) AMF structures or in situ visualization of their enzymatic activities. In recent studies, however, imaging of non-fixed root samples by means of fluorescent molecular markers of the symbiotic process has been used to improve our understanding of colonization dynamics at the cellular level. As many parts of the molecular mechanism implicated in AM symbiosis are common to nodule symbiosis, several molecular markers are available in the model legume plants,
Rice (
Transcriptome analysis of mycorrhized rice roots revealed that an AM-specific marker gene of rice,
The concept that mycorrhization is linked to the successive formation of infection units is supported by the observation that decreased hyphopodium formation leads to decreased mycorrhization. Under low-phosphate conditions, roots secrete strigolactones (SLs), which are carotenoid-derived phytohormones. A chemical analog of SLs, GR-24, activated mitochondrial respiratory activity and facilitated hyphal branching of
In the field, multiple AMFs, from different species, can co-colonize roots, with multiple AMF species being detectable in only a 1-cm-long root fragment [56]. Thus, field roots can be regarded as a mosaic of the various functionalities of the different AMFs [57]; alternatively, only a portion of the AMF infection unit colonizing the roots may temporarily contribute to particular functions in response to specific environmental conditions [58]. However, the dynamics of the functionality of the respective AMFs in field roots have been little studied. Abiotic and biotic factors may influence the AMF composition, at least over a long time period [59], but the short-term effects of such environmental factors may also influence the various active (functional) AMFs as well as the functionality of the mycorrhiza as an entirety under field conditions. For example, not all infection units containing fine-branched arbuscules in roots grown in field soils are metabolically active (Figure 3) [60]. Further study will be needed to understand the functional dynamics of field mycorrhizas by considering infection unit-based colonization dynamics.
3. Conclusion
Our understanding of the molecular mechanism underlying the plant nutrient uptake system has been greatly advanced by the use of molecular studies and genetics. These studies have been based almost entirely on the plant alone. However, the plant nutrient uptake system is largely dependent on the largely undiscovered functionalities of diverse soil microorganisms. Roots of plants in the field are generally colonized with a range of different AMFs, but the functionality of these individual species is largely unknown. In addition, the genetic structure of AMF is quite enigmatic [41]. Recent studies into single-nucleus sequencing of some AMF culture lines demonstrated the presence of not only homokaryons but also dikaryons and heterokaryons [61, 62]. Furthermore, long-read whole-genome sequencing of
As mentioned before, AM infection units have a short life span and collapse within a few days, at least in the live imaging of rice seedlings [36, 37]. The development of mycorrhizal roots is associated with the turnover and de novo colonization by new AMFs, providing the opportunity to allow different AMF species to colonize the roots, depending on the context (environmental factors, plant growth stage, nutrition, etc.). Accordingly, field mycorrhizal roots can comprise multiple functionalities with different AMF species.
Plant breeding programs are not able to select for the genomic properties of plants adapted to all field conditions (soil type, water content, nutrient level, climate, etc.). On the other hand, plant roots closely interact with the native fungal partners that may have genetically recorded beneficial traits for adapting to the local environment. The specific phenotype (functionality) of native AMFs may be conferred by accessory genes that are not shared by all members of a species [64]. However, due to the complexity of the genetic basis of AMF individuals, it is difficult to understand which AMF genes are really functional in the roots. In a model plant (e.g., rice), the thin root cortex would allow us to isolate the genetic information of AMF individuals in the form of the infection unit. Furthermore, rice roots are technically suitable for detecting metabolic activities by means of vital staining. Furthermore, transgenic rice producing fluorescent molecular markers (e.g., phosphate transporter, GFP) is available to assess the functionality of the AMFs in situ. Thus, future studies should focus on the functionality of field AMF individuals, with emphasis on the genetic information and the dynamic functionality.
Acknowledgments
This work was supported partly by the Japan Science and Technology Agency [ACCEL grant No. JPMJAC1403].
References
- 1.
Trappe JM. Selection of fungi for ectomycorrhizal inoculation in nurseries. Annual Review of Phytopathology. 1977; 15 :203-222 - 2.
Smith SE, Read DJ. Mycorrhizal Symbiosis. Cambridge, UK: Academic Press; 2008 - 3.
Wang B, Qiu Y. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza. 2006; 16 :299-363. DOI: 10.1007/s00572-005-0033-6 - 4.
Balestrini R, Bonfante P. Cell wall remodeling in mycorrhizal symbiosis: A way towards biotrophism. Frontiers in Plant Science. 2014; 5 :237 - 5.
Strullu-Derrien C, Selosse MA, Kenrick P, Martin FM. The origin and evolution of mycorrhizal symbioses: From palaeomycology to phylogenomics. The New Phytologist. 2018; 220 :1012-1030 - 6.
Dickson S, Smith FA, Smith SE. Structural differences in arbuscular mycorrhizal symbioses: More than 100 years after Gallaud, where next? Mycorrhiza. 2007; 17 :375-393 - 7.
Smith SE, Smith FA. Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales. Annual Review of Plant Biology. 2011; 62 :227-250 - 8.
Bücking H, Liepold E, Ambilwade P. The role of the mycorrhizal symbiosis in nutrient uptake of plants and the regulatory mechanisms underlying these transport processes. Plant Science. 2012; 4 :108-132. DOI: 10.5772/52570 - 9.
Luginbuehl LH, Oldroyd GE. Understanding the arbuscule at the heart of endomycorrhizal symbioses in plants. Current Biology. 2017; 27 :R952-R963 - 10.
MacLean AM, Bravo A, Harrison MJ. Plant signaling and metabolic pathways enabling arbuscular mycorrhizal symbiosis. The Plant Cell. 2017; 29 :2319-2335 - 11.
Choi J, Summers W, Paszkowski U. Mechanisms underlying establishment of arbuscular mycorrhizal symbioses. Annual Review of Phytopathology. 2018; 56 :135-160 - 12.
Lanfranco L, Fiorilli V, Gutjahr C. Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis. The New Phytologist. 2018; 220 :1031-1046. DOI: 10.1111/nph.15230 - 13.
Ligrone R, Carafa A, Lumini E, Bianciotto V, Bonfante P, Duckett JG. Glomeromycotean associations in liverworts: A molecular, cellular, and taxonomic analysis. American Journal of Botany. 2007; 94 :1756-1777 - 14.
Rimington WR, Pressel S, Duckett JG, Field KJ, Read DJ, Bidartondo MI. Ancient plants with ancient fungi: Liverworts associate with early-diverging arbuscular mycorrhizal fungi. Proceedings of the Royal Society B. 2018; 285 :pii: 20181600. DOI: 10.1098/rspb.2018.1600 - 15.
Delaux PM, Radhakrishnan GV, Jayaraman D, Cheema J, Malbreil M, Volkening JD, et al. Algal ancestor of land plants was preadapted for symbiosis. Proceedings of the National Academy of Sciences of the United States of America. 2015; 112 :13390-13395 - 16.
Engel R, Szabó K, Abrankó L, Rendes K, Füzy A, Takács T. Effect of arbuscular mycorrhizal fungi on the growth and polyphenol profile of marjoram, lemon balm, and Marigold. Journal of Agricultural and Food Chemistry. 2016; 64 :3733-3742 - 17.
Rozpądek P, Rąpała-Kozik M, Wężowicz K, Grandin A, Karlsson S, Ważny R, et al. Arbuscular mycorrhiza improves yield and nutritional properties of onion ( Allium cepa ). Plant Physiology and Biochemistry. 2016;107 :264-272 - 18.
Srivastava S, Conlan XA, Cahill DM, Adholeya A. Rhizophagus irregularis as an elicitor of rosmarinic acid and antioxidant production by transformed roots ofOcimum basilicum in an in vitro co-culture system. Mycorrhiza. 2016;26 :919-930 - 19.
Plett JM, Martin FM. Know your enemy, embrace your friend: Using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms. The Plant Journal. 2018; 93 :729-746 - 20.
Ohsowski BM, Zaitsoff PD, Öpik M, Hart MM. Where the wild things are: Looking for uncultured glomeromycota. The New Phytologist. 2014; 204 :171-179 - 21.
Vierheilig H, Ocampo JA. Relationship between SDH-activity and VA-mycorrhizal infection. Agriculture, Ecosystems and Environment. 1990; 29 :439-442 - 22.
Hamel C, Fyles H, Smith DL. Measurement of development of endomycorrhizal mycelium using three different vital stains. The New Phytologist. 1990; 115 :297-302 - 23.
Kobae Y. Dynamic phosphate uptake in arbuscular mycorrhizal roots under field conditions. Frontiers in Environmental Science. 2019; 6 :159 - 24.
Gallaud I. Études sur les mycorrhizes endotrophes. Revue Générale de Botanique. 1905; 17 :5-48, 66-83, 123-136, 223-239, 313-325,, 378, 425-433, 479-500 - 25.
Cox G, Sanders F. Ultrastructure of the host–fungus interface in a vesicular-arbuscular mycorrhiza. The New Phytologist. 1974; 73 :901-912 - 26.
Cox G, Tinker PB. Translocation and transfer of nutrients in vesicular-arbuscular mycorrhizas. The New Phytologist. 1976; 77 :371-378 - 27.
Bonfante-Fasolo P. Anatomy and morphology of VA mycorrhizae. In: Powell CL, Bagyaraj DJ, editors. VA Mycorrhizas. Boca Raton, FL: CRC Press; 1984. pp. 5-33 - 28.
Alexander T, Meier R, Toth R, Weber HC. Dynamics of arbuscule development and degeneration in mycorrhizas of Triticum aestivum L. andAvena sativa L. with reference toZea mays L. The New Phytologist. 1988;110 :363-370 - 29.
Alexander T, Toth R, Meier R, Weber HC. Dynamics of arbuscule development and degeneration in onion, bean, and tomato with reference to vesicular-arbuscular mycorrhizae in grasses. Canadian Journal of Botany. 1989; 67 :2505-2513 - 30.
Zipfel C, Oldroyd GE. Plant signalling in symbiosis and immunity. Nature. 2017; 543 :328 - 31.
Pimprikar P, Gutjahr C. Transcriptional regulation of arbuscular mycorrhiza development. Plant and Cell Physiology. 2018; 59 :678-695 - 32.
Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ. A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America. 2007;104 :1720-1725 - 33.
Yang SY, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, et al. Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter1 gene family. The Plant Cell. 2012;24 :4236-4251 - 34.
Floss DS, Gomez SK, Park HJ, MacLean AM, Müller LM, Bhattarai KK, et al. A transcriptional program for arbuscule degeneration during AM symbiosis is regulated by MYB1. Current Biology. 2017; 27 :1206-1212 - 35.
Li C, Zhou J, Wang X, Liao H. A purple acid phosphatase, GmPAP33 , participates in arbuscule degeneration during arbuscular mycorrhizal symbiosis in soybean. Plant, Cell and Environment. 2019;42 (6):2015-2027. DOI: 10.1111/pce.13530 - 36.
Kobae Y, Hata S. Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. Plant and Cell Physiology. 2010; 51 :341-353 - 37.
Kobae Y, Fujiwara T. Earliest colonization events of Rhizophagus irregularis in rice roots occur preferentially in previously uncolonized cells. Plant and Cell Physiology. 2014;55 :1497-1510 - 38.
Mosse B. Specificity in VA mycorrhizas. In: Endomycorrhizas. London, UK: Academic Press; 1975. pp. 469-484 - 39.
McGonigle TP, Fitter AH. Ecological specificity of vesicular-arbuscular mycorrhizal associations. Mycological Research. 1990; 94 :120-122 - 40.
Buwalda JG, Stribley DP, Tinker PB. The development of endomycorrhizal root systems. V. The detailed pattern of development of infection and the control of infection level by host in young leek plants. The New Phytologist. 1984; 96 :411-427 - 41.
Bruns TD, Corradi N, Redecker D, Taylor JW, Öpik M. Glomeromycotina: What is a species and why should we care? New Phytologist. 2018; 220 :963-967. DOI: 10.1111/nph.14913 - 42.
Öpik M, Davison J. Uniting species-and community-oriented approaches to understand arbuscular mycorrhizal fungal diversity. Fungal Ecology. 2016; 24 :106-113 - 43.
Kobae Y, Tamura Y, Takai S, Banba M, Hata S. Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant and Cell Physiology. 2010; 51 :1411-1415 - 44.
Kobae Y, Gutjahr C, Paszkowski U, Kojima T, Fujiwara T, Hata S. Lipid droplets of arbuscular mycorrhizal fungi emerge in concert with arbuscule collapse. Plant and Cell Physiology. 2014; 55 :1945-1953 - 45.
Roth R, Hillmer S, Funaya C, Chiapello M, Schumacher K, Lo Presti L, et al. Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules. Nature Plants. 2019; 5 :204 - 46.
Güimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, et al. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonisation. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102 :8066-8070 - 47.
Gutjahr C, Banba M, Croset V, An K, Miyao A, An G, et al. Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. The Plant Cell. 2008; 20 :2989-3005 - 48.
Kobae Y, Kameoka H, Sugimura Y, Saito K, Ohtomo R, Fujiwara T, et al. Strigolactone biosynthesis genes of rice are required for the punctual entry of arbuscular mycorrhizal fungi into the roots. Plant and Cell Physiology. 2018; 59 :544-553 - 49.
Akiyama K, Matsuzaki KI, Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature. 2005; 435 :824 - 50.
Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, et al. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biology. 2006; 4 :e226 - 51.
Salvioli A, Ghignone S, Novero M, Navazio L, Venice F, Bagnaresi P, et al. Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. The ISME Journal. 2016; 10 :130-144 - 52.
Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, et al. Strigolactone inhibition of shoot branching. Nature. 2008; 455 :189-194 - 53.
Koltai H, LekKala SP, Bhattacharya C, Mayzlish-Gati E, Resnick N, Wininger S, et al. A tomato strigolactone-impaired mutant displays aberrant shoot morphology and plant interactions. Journal of Experimental Botany. 2010; 61 :1739-1749 - 54.
Vogel JT, Walter MH, Giavalisco P, Lytovchenko A, Kohlen W, Charnikhova T, et al. SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. The Plant Journal. 2010; 61 :300-311 - 55.
Yoshida S, Kameoka H, Tempo M, Akiyama K, Umehara M, Yamaguchi S, et al. The D3 F-box protein is a key component in host strigolactone responses essential for arbuscular mycorrhizal symbiosis. The New Phytologist. 2012; 196 :1208-1216 - 56.
van Tuinen D, Jacquot E, Zhao B, Gollotte A, Gianinazzi-Pearson V. Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25S rDNA-targeted nested PCR. Molecular Ecology. 1988; 7 :879-887 - 57.
Jansa J, Smith FA, Smith SE. Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? The New Phytologist. 2008; 177 :779-789 - 58.
Compant S, van der Heijden MG, Sessitsch A. Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiology Ecology. 2010; 73 :197-214 - 59.
Xu X, Chen C, Zhang Z, Sun Z, Chen Y, Jiang J, et al. The influence of environmental factors on communities of arbuscular mycorrhizal fungi associated with Chenopodium ambrosioides revealed by MiSeq sequencing investigation. Scientific Reports. 2017;7 :45134 - 60.
Kobae Y, Ohtomo R, Oka N, Morimoto S. A simple model system for identifying arbuscular mycorrhizal fungal taxa that actively colonize rice ( Oryza sativa L.) roots grown in field soil. Soil Science & Plant Nutrition. 2017;63 :29-36 - 61.
Ropars J, Toro KS, Noel J, Pelin A, Charron P, Farinelli L, et al. Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi. Nature Microbiology. 2016; 1 :16033 - 62.
Chen EC, Mathieu S, Hoffrichter A, Sedzielewska-Toro K, Peart M, Pelin A, et al. Single nucleus sequencing reveals evidence of inter-nucleus recombination in arbuscular mycorrhizal fungi. eLife. 2018; 7 :e39813 - 63.
Maeda T, Kobayashi Y, Kameoka H, Okuma N, Takeda N, Yamaguchi K, et al. Evidence of non-tandemly repeated rDNAs and their intragenomic heterogeneity in Rhizophagus irregularis . Communications Biology. 2018;1 :87 - 64.
Mathieu S, Cusant L, Roux C, Corradi N. Arbuscular mycorrhizal fungi: Intraspecific diversity and pangenomes. The New Phytologist. 2018; 220 :1129-1134 - 65.
Kobae Y, Ohtomo R. An improved method for bright-field imaging of arbuscular mycorrhizal fungi in plant roots. Soil Science & Plant Nutrition. 2016; 62 :27-30. DOI: 10.1080/00380768.2015.1106923 - 66.
MacDonald RM, Lewis M. The occurrence of some acid phosphatases and dehydrogenases in the vesicular-arbuscular mycorrhizal fungus Glomus mosseae . New Phytologist. 1978;80 :135-141. DOI: 10.1111/nph.1978.80.issue-1 - 67.
Fiorilli V, Vallino M, Biselli C, Faccio A, Bagnaresi P, Bonfante P. Host and non-host roots in rice: Cellular and molecular approaches reveal differential responses to arbuscular mycorrhizal fungi. Frontiers in Plant Science. 2015; 6 :636. DOI: 10.3389/fpls.2015.00636 - 68.
Gutjahr C, Sawers RJH, Marti G, Andrés-Hernández L, Yang SY, Casieri L, et al. Transcriptome diversity among rice root-types during asymbiosis and interaction with arbuscular mycorrhizal fungi. Proceedings of the National Academy of Sciences of the United States of America. 2015; 112 :6754-6759. DOI: 10.1073/pnas.1504142112