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Genetic Diversity and Structure of Neotyphodium Species and Their Host Achnatherum Sibiricum in a Natural Grass–Endophyte System

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Genetic Diversity and Structure of Neotyphodium Species and Their Host Achnatherum Sibiricum in a Natural Grass–Endophyte System Microb Ecol (2010) 59:744–756 DOI 10.1007/s00248-010-9652-3 PLANT MICROBE INTERACTIONS Genetic Diversity and Structure of Neotyphodium Species and Their Host Achnatherum sibiricum in a Natural Grass–Endophyte System Xin Zhang & Anzhi Ren & Huacong Ci & Yubao Gao Received: 8 June 2009 /Accepted: 26 February 2010 /Published online: 30 March 2010 # Springer Science+Business Media, LLC 2010 Abstract Achnatherum sibiricum (Poaceae) is a perennial even when their gene flows do not match each other. bunchgrass native to the Inner Mongolia Steppe of China. Furthermore, we suggested that the same genotype of This grass is commonly infected by epichloë endophytes endophyte as well as host should be confirmed if the with high-infection frequencies. Previously, we identified objective of the study is to know the influence of endophyte two predominant Neotyphodium spp., N. sibiricum and N. or host genotype on their symbiotic relationship, instead of gansuense. In the present study, genetic diversity and just considering whether the plant is infected by an structure were analyzed for the two predominant Neo- endophyte or not, since endophytes from the same host typhodium spp. as well as the host grass. We obtained 103 species could exhibit high levels of genetic diversity, which fungal isolates from five populations; 33 were identified as is likely to influence the outcome of their symbiotic N. sibiricum and 61 as N. gansuense. All populations relationship. hosted both endophytic species, but genetic variation was much higher for N. gansuense than for N. sibiricum. The majority of fungal isolates were haploid, and 13% of them Introduction were heterozygous at one SSR locus, suggesting hybrid origins of those isolates. Significant linkage disequilibrium The Epichloë spp. and their asexual descendants Neo- of fungal SSR loci suggested that both fungal species typhodium spp.—collectively called epichloë endophytes— primarily propagate by clonal growth through plant seeds, comprise a group of filamentous fungi (Clavicipitaceae, whereas variation in genetic diversity and the presence of Ascomycota) that form symbiotic infection within many hybrids in both endophytic species revealed that although cool-season grasses [20]. The Epichloë species typically clonal propagation was prevalent, occasional recombination exhibit a sexual stage with the development of stromata might also occur. By comparing genetic differentiation around the base of plant flag leaf followed by the among populations, we found around 4–7-fold greater reproductive sterilization of the host, often known as plant differentiation of endophyte populations than host popula- choke disease [53, 54]. However, in the asexual stage of tions, implying more restricted gene flow of endophytes Epichloë spp. and all Neotyphodium spp., the fungus does than hosts. We proposed that endophyte infection of A. not produce any external structure and is transmitted sibiricum might confer the host some selective advantages through seeds of infected plants [43]. under certain conditions, which could help to maintain The symbiosis between epichloë endophytes and their high-endophyte-infection frequencies in host populations, hosts has been suggested to range from antagonistic to mutualistic [32, 38]. Some obligate horizontally transmitted Epichloë spp. are more likely to be antagonistic to the host Xin Zhang and Anzhi Ren contributed equally to this work. : : : because the reproduction of the host is aborted upon X. Zhang A. Ren H. Ci Y. Gao (*) formation of stromata, whereas many vertically transmitted Department of Plant Biology and Ecology, Neotyphodium spp. are proposed as plant mutualists since College of Life Sciences, Nankai University, Tianjin 300071, People’s Republic of China the fitness of the endophyte and the host is closely related e-mail: [email protected] [42]. Early studies of grass–endophyte associations using Diversity and Structure of Endophytes and Host 745 two economically important grass species, Lolium perenne order to predict their symbiotic relationship, the ecological and L. arundinaceum (= Schedonorus arundinaceus= dynamics of the plant communities as well as their Festuca arundinacea) suggested that endophytes were evolutionary processes. plant-defending mutualists [11, 41]. The benefits conferred In China, there have been few studies on endophytic to host by the endophyte are well understood, which fungi associated with native grasses, despite the fact that typically include protection from mammalian and insect many grass species have been found to be infected by herbivory [5, 27], disease resistance [25], stress tolerance endophytes [51]. The most studied grass is Achnatherum [2] and improved growth and reproduction [29, 35]. For inebrians, a widely distributed endophyte-infected grass native grass–endophyte associations, however, their inter- notorious for its toxicity to livestock [6]. In our previous actions are more variable. In some grass species, endophyte extensive survey in the Inner Mongolia Steppe of China, infection could benefit their hosts under stress conditions another species, A. sibiricum (L.) was also found to be [6, 12, 24, 29, 33, 44], while in other studies, endophyte- commonly infected by epichloë endophytes with high- infected grasses do not appear to be competitive over those infection frequency [51]. In a previous study, N. sibiricum that are endophyte free [17, 18]. In natural populations, the and N. gansuense were identified as two predominant costs and benefits of harboring endophytes may vary with endophytic species in A. sibiricum populations [56]. The genotype of both plant and endophyte, as well as with objective of the present study is to further evaluate the environmental conditions [32, 38]. Among those factors genetic diversity and population genetic structure of the two that may influence the outcome of endophyte–grass predominant Neotyphodium spp. in different A. sibiricum interactions, endophyte genotype and the interacting host populations, as well as the relationship of genetic differenti- genotype has proved to be most critical [30]. ation and geographical distance between populations. Further- It is reported that in native grass populations, endophytic more, we compared the genetic structure of the host and fungal communities may be more diverse and variable than endophytes to better understand the movement of genes and that of agronomic and economically important species [45]. how this movement may influence population genetic struc- This reflects on the endophyte species diversity, and also ture and therefore the co-evolution of the host and endophytes. the endophyte morphological and genetic diversities [9, 10, 13, 45]. For example, only one fungal genotype was transmitted through an economically important cultivar of Materials and Methods tall fescue, Kentucky 31 (KY-31) [39]. In contrast, considerable morphological, physiological and biochemical Sampling of the Plant Materials variations were observed among endophytic isolates grown from native tall fescue collected worldwide [10, 34]. In In a previous extensive survey, A. sibiricum was found at only another endophyte-infected native grass, Arizona fescue eight geographical locations in the Inner Mongolia Steppe (Festuca arizonica), >400 different fungi were isolated [51]. In the present study, A. sibiricum from five natural from five Arizona fescue populations, which might rival populations, IMGERS-CAS, Xi Ujimqin Qi, Huolingol, fungal diversity in woody plants [45]. In the study of ArshanandHailarinthemid-andeasternInner endophyte genetic diversity, marked genetic variation has Mongolia Steppe were chosen (Fig. 1). Populations were been detected in several epichloë species studied, including selected from the western most distribution of A. sibiricum E. festucae from F. rubra and Festuca subg. Festuca, N. to the east and covered various plant community types, lolii from L. perenne and N. starrii from F. arizonica [3, 14, including meadow steppe, typical steppe and forest edge. 46, 50]. There are several processes by which endophytes Plant material was collected in July 2006. Within each could obtain their genetic variation, which typically include population, 22 (Xi Ujimqin Qi) to 31 (Hailar) plant sexual reproduction of Epichloë spp., interspecific hybrid- individuals were randomly chosen along a line transect. ization of Neotyphodium spp., as well as mitotic or The distance between sampled plant individuals was at parasexual recombination and mutation accumulation [13, least 5 m to minimize the probability of sampling ramets 28, 46, 49, 50]. Moreover, studies of their population belonging to the same genet. Leaves of each plant were genetic structure detected much higher levels of population harvested and stored in silica gel in locked bottles before differentiation of E. festucae than N. starrii. The occasional transporting back to the laboratory for DNA extraction. sexual reproduction and sporulation may facilitate gene Seeds from each plant were collected in September 2006 flow among endophyte populations and thus reduce and deposited in separate envelopes for fungal endophyte population differentiation level of E. festucae [3, 46, 50]. detection and isolation. Only one stroma each was found Considering the influence of endophyte genotype on the for the Xi Ujimqin Qi, Huolingol and Arshan populations, performance of the symbiont, it is important to determine separately, after screening several hundred plant individuals in the diversity of the endophyte
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