Yutao Wang, E-mail:
#并列第一作者
#These authors contributed equally to this work
丛枝菌根真菌(AMF)在自然界分布广泛,能与大部分维管植物的根系形成菌根共生体。它们在调节植物群落结构和全球的碳、氮、磷循环等方面发挥着重要的生态功能,也是农林、环境领域最具应用前景的微生物类群。受限于培养方法、研究手段等,长期以来对AMF基因组、转录组特征的认识非常有限。最近10年,AMF基因组和转录组的相关研究在高通量测序技术的推动下取得了较快发展;研究结果也显著提高了对AMF遗传发育、代谢生理、共生机制等的认识。本文综述了目前已完成测序的AMF种类的基因组、转录组信息。结果发现,已测序的AMF种类普遍具有基因组大、转座子丰富、AT碱基含量高、含大量未知功能基因与特异性基因、缺少部分共生相关基因等特点。在转录层面,总结了不同AMF种类、AMF不同共生结构、共生阶段以及与不同寄主植物共生时的转录本特征。结果发现,不同种类AMF的转录本大小差异明显。不同共生阶段或不同共生结构中的AMF转录本也具有较大的差异,且差异表达的基因大部分与养分交易、信号转导等密切相关。相比之下,同种AMF与不同寄主植物共生时的转录本表现出较高的保守性。最后,本文提出了本领域需要重点关注的研究方向,包括AMF纯培养技术的革新、AMF基因功能的解析、非模式AMF类群的研究以及对AMF蛋白组的研究。
Arbuscular mycorrhizal fungi (AMF) are widely distributed in nature and can form mycorrhizal symbiosis with the roots of most vascular plants. They play important ecological roles in the regulation of plant community, and are deeply involved in the global carbon, nitrogen, and phosphorus cycling. They are also the most promising microbial groups in the fields of agriculture, forestry and environment. However, so far the information of their genomic and transcriptomic characters was limited, partially due to the technique limitations in their cultivation. In the past decade, researches on AMF genome and transcriptome have achieved a rapid development under the impetus of high-throughput sequencing. These studies have greatly improved our understanding of AMF in heredity, development, metabolic physiology and symbiosis mechanisms. Here we reviewed the research progresses in the available genomic and transcriptomic information of AMF based on published literature. We found that genomes of available AMF species commonly have large sizes, high transposon abundances, high GC contents, rich in functionally-unknown and species-specific genes, and are lack of some symbiosis-related genes. We also summarized the transcriptomic characteristics of AMF in different symbiotic structures, at different symbiosis stages and with different host plants. The results showed that the transcriptomic sizes generally varied among different AMF species. Also, in different symbiotic structures or at different symbiotic stages, diverse transcriptomic characteristics were found, especially for the expression profiles of genes related to nutrient exchange and signal transduction. In contrast, the transcripts of the same AMF in symbiosis with different host plants were relatively conserved. Finally, we proposed the research directions that need to be focused on in this field, including the innovation of AMF asymbiotic culture technology, the analysis of AMF gene functions, the study of non-model AMF groups and the study of AMF proteome.
丛枝菌根真菌(arbuscular mycorrhizal fungi,AMF)是自然界分布最广泛、最重要的土壤微生物类群之一,能与大约80%的陆生植物以及大部分的水生、半水生植物形成共生关系[
AMF研究的传统方法主要包括菌根形态学的观察[
基因组学、转录组学技术对揭示AMF与寄主植物共生的机制非常重要,但目前对于AMF基因组、转录组的认识仍然非常有限,这主要有两方面原因:一方面,AMF长期以来被认为是一种高度依赖寄主植物碳源的共生菌,无法在脱离寄主根系的情况下实现纯培养,而在传统土壤培养条件下又很难获得足够纯净的AMF菌丝及孢子。利用单孢建立起来的AMF与转基因胡萝卜(
[
由于早期的研究者对原囊菌目和类球囊菌目的分类有一定争议,且尚缺乏针对这两个目的活体培养技术[
已测序AMF及来自
Genome information for sequenced AMF and non-AMF species in
Species | Genome/Mb | Genes | GC/% | RS/% | TEs | NCBI No. & Ref. |
AMF materials used for sequencing were mostly cultured in the monoxenic root organ cultures, except | ||||||
Glomerales | ||||||
|
125.9 | 26659 | 27.25 | 19.61 | 17115 | PRJNA299202 [ |
138.3 | 25760 | 27.19 | 20.48 | 19382 | PRJNA299206 [ |
|
131.5 | 26585 | 27.19 | 21.98 | 19345 | PRJNA299208 [ |
|
124.9 | 25164 | 27.22 | 19.86 | 16840 | [ |
|
123.0 | 26756 | 27.26 | 18.54 | 17334 | PRJNA299212 [ |
|
136.8 | 26183 | 27.53 | 21.72 | 14451 | PRJNA208392 [ |
|
146.5 | 29805 | 21.40 | NA | 17710 | PRJNA477348 [ |
|
131.0 | NA | 25.80 | NA | NA | PRJNA565846 | |
149.8 | 43674 | 27.90 | NA | NA | PRJDB4945 | |
|
136.9 | 21158 | 26.55 | 31.66 | 883 | PRJNA430010 [ |
170.9 | NA | NA | NA | NA | PRJNA477348 | |
|
125.9 | 23252 | 27.19 | 23.19 | 483 | [ |
|
116.4 | 27753 | 27.20 | 36.04 | NA | PRJDB6444 [ |
|
125.9 | 23014 | 23.80 | NA | NA | PRJNA430014 |
Diversisporales | ||||||
|
156.6 | 28348 | 32.00 | 43.60 | NA | PRJNA431769 [ |
|
598.0 | 31291 | 28.81 | 63.44 | 10422 | PRJNA430513 [ |
|
773.1 | 26603 | 27.68 | 64.00 | NA | PRJNA575165 [ |
Mortierellales | ||||||
|
49.9 | 14969 | 48.05 | 4.63 | 167 | PRJNA346817 [ |
|
38.4 | 12796 | 51.72 | NA | 6277 | ADAG00000000 [ |
Mucorales | ||||||
|
36.6 | 11719 | 35.78 | 9.74 | 2319 | AMYB00000000 [ |
|
53.9 | 16528 | 26.55 | 24.77 | 857 | AMYC00000000 [ |
基于已有的测序数据,AMF基因组(基于单个细胞内所有的核)大小在116-773 Mb之间,显著大于来自于毛霉菌门中的被孢霉亚门和毛霉菌亚门中的腐生真菌基因组(36-54 Mb)[
AMF较大的基因组可能与其含有大量重复基因(duplicated genes)有关。Chen等(2018)和Morin等(2019)发现AMF基因组中的核心基因(定义为所有已测序AMF都共有的基因)、非必需基因(定义为至少在2个而非所有AMF菌株中存在的基因)和特异性基因(定义为只在单株AMF中出现的基因)都存在不同程度的复制[
AMF基因组具有较高的AT碱基含量(AT%)。例如,异形根孢囊霉DAOM197198基因组内AT%为72%,玫瑰红巨孢囊霉的AT%为71%[
AMF的基因组具有高丰度的转座子。比如,异形根孢囊DAOM197198基因组内转座子覆盖率(coverage)可达36%,玫瑰红巨孢囊霉的转座子覆盖率甚至达到63%[
大量未知功能基因的存在是AMF基因组的又一典型特征。目前,一般微生物基因组中可被注释的基因通常占到全部基因的90%以上[
AMF的基因组内存在大量的高度特异性基因(分为物种层面和菌株层面);某些物种的特异性基因占比高达64%(如玫瑰红巨孢囊霉),远高于其姊妹门的其他真菌[
AMF具有部分与姊妹门腐生菌同源的保守基因,这类基因主要编码一些涉及初级代谢和信号转导途径的相关蛋白,例如酪氨酸激酶(tyrosine kinase),表明AMF在基础代谢方面保留了部分与腐生菌相同的方式[
植物细胞壁降解酶基因的丢失是AMF基因组研究中一个重要的发现。作为一种能够侵染植物根系并在寄主根细胞内定殖的真菌,这类基因的丢失似乎是不合理的。植物细胞壁一般含有纤维素、半纤维素等多糖。AMF要实现对寄主的侵染似乎需要借助参与多糖降解的碳水化合物活化酶,包括在多糖降解过程中发挥主要作用的多糖水解酶(glycoside hydrolases,GH)[
与AMF相比,同属于内生菌根(endomycorrhiza)的兰科菌根(orchid mycorrhiza)和欧石南菌根(ericoid mycorrhiza)就拥有数量较多的植物细胞壁降解酶。以Miyauchi等(2020)的研究为例,兰科菌根所含的相关基因平均数目约为114,杜鹃类菌根真菌所含相关基因的平均数目约为49。而无法定殖到寄主植物细胞内的外生菌根所含有的植物细胞壁降解酶数量就很少,涉及纤维素和木质素降解的基因平均数目仅有11个左右[
植物细胞壁降解酶的缺失可能是AMF对严格共生生活方式的一种适应性演化,用以防止被寄主植物的病原物关联的分子模式(pathogen-associated molecular patterns,PAMP)和损伤相关分子模式(damage-associated molecular patterns,DAMP)等防御机制识别,进而减少寄主免疫系统相关效应因子的释放,实现与寄主共生的目的[
脂质是AMF的重要组分,Bago (2004)曾将AMF定义为“产油”真菌,因为其干重的25%均由脂质组成[
早期研究表明,AMF的萌发孢子以及外生菌丝无法合成长链脂肪酸,仅在与植物共生的结构(根内菌丝)中才有长链脂肪酸的存在[
长久以来,AMF都被认为是一种进行无性生殖的微生物。随着研究的不断深入,人们陆续发现AMF的基因组内存在着与其他真菌有性生殖基因同系的基因,包括减数分裂的特异性基因[
作为一种与大部分维管植物有着密切共生关系的微生物,AMF在驱动全球C、N、P等元素的大循环中发挥着重要的作用。AMF基因组中与这些营养元素循环相关的基因及其作用也一直备受关注。
长久以来,AMF一直被认为是一种严格依赖寄主植物获取C源的微生物。由于缺乏蔗糖酶等有机质分解酶的基因[
AMF促进寄主植物P获取能力是AMF最基本、最重要的功能。自然土壤中的P大多为结合态。尽管AMF的基因组内存在编码磷酸酶的基因,包括对硝基苯酚磷酸酶、酸性磷酸酶和碱性磷酸酶等[
总体而言,AMF基因组学的研究已经深度拓展了我们对AMF的认识;尤其是为揭示AMF的演化历史、营养类型、生活方式等方面提供了丰富而重要的信息,也为AMF的其他方面研究提供了重要的指导。不过,由于AMF纯培养和测序技术等方面的限制,目前已知的AMF基因组信息仍然非常有限,亟需更多关于AMF基因组学的研究,尤其是针对来自原囊菌目和类球囊菌目的基因组学研究。
NCBI数据库中目前已经囊括AMF全部4个目(多孢囊菌目、球囊菌目、原囊菌目和类球囊菌目)中的1个或多个种类的转录组信息。其中,多胞囊菌目和球囊菌目分别有6个和5个种的转录组信息,而原囊菌目和类球囊菌目则只有1个种有转录组信息(
转录组测序的AMF物种及测序信息
AMF species and sequencing information for transcriptome sequencing
Species | Method | Object | Transcripts | GC/% | Unannotated/% | NCBI No. & Ref. |
*: genome sequence available. | ||||||
|
Single-cell transcriptome | Quiescent spores | 139347 | 43 | 56.7 | PRJNA376430 [ |
|
Single-cell transcriptome | Quiescent spores | 49516 | 43 | 48.6 | PRJNA376430 [ |
|
Single-cell transcriptome | Quiescent spores | 207252 | 47 | 48.1 | PRJNA376430 [ |
|
Transcriptome | Germinating spores and hyphae | 86183 | 32 | 87.3 | PRJNA267628 [ |
|
Transcriptome | Hyphae and spores | 86332 | 33 | 82.0 | PRJNA281451 [ |
|
Single-cell transcriptome | Quiescent spores | 57737 | 33 | 71.0 | PRJNA376430 [ |
|
Single-cell transcriptome | Quiescent spores | 28680 | 33 | 41.7 | PRJNA376430 [ |
|
Single-cell transcriptome | Quiescent spores | 36227 | 30 | 64.7 | PRJNA376430 [ |
|
Single-cell transcriptome | Quiescent spores | 56258 | 33 | 60.9 | PRJNA376430 [ |
|
Transcriptome | Germinating hyphae | NA | 36 | NA | PRJNA209039 |
|
Transcriptome | Hyphae and spores | 39663 | 37 | NA | [ |
|
Transcriptome | Germinating spores and hyphae | 25906 | 34 | 58.2 | PRJNA274445 [ |
|
Single-cell transcriptome | Quiescent spores | 101297 | 41 | 60.5 | PRJNA376430 [ |
与基因组情况类似,AMF转录组中也包含了大量功能未被注释的部分(
作为一种能够快速适应环境变化的菌根类型,AMF具有高度的物种特异性;在转录层面上表现为种间和种内基因表达的差异,且这种差异在不同的分类水平上具有不同的呈现[
不同AMF种类的差异主要体现在转录组的大小上。以最常研究的球囊菌目和多胞囊菌目为例,多胞囊菌目内玫瑰红巨孢囊霉转录本的数目可以达到球囊菌目内异形根孢囊霉转录本数目的3倍以上(
同种但不同菌株的AMF转录组之间可能也具有较大的差异。以已完成测序的AMF菌株最多的异形根孢囊霉为例,DAOM197198菌株中含有更多涉及信号通路的TKL蛋白,而菌株A1能够表达数量更多的ABC转运蛋白、脂肪酸去饱和酶和氨基酸转移酶;C2菌株能够表达更多的金属还原蛋白,A5菌株则能够表达更多的离子结合蛋白和转录因子IID (TEIID)的转录起始因子,以及RNA识别基元(motifs)和BED型锌指细胞调节因子。A4菌株的泛素和组蛋白结构域表达不足,而B3菌株则缺乏热休克蛋白Hsp70和氨基糖苷磷酸转移酶[
AMF的共生过程可以分为3个阶段:(1) 非共生阶段,短时间内孢子自主萌发和菌丝独立发育的阶段;(2) 前共生阶段,孢子受到寄主植物根系分泌的信号诱导后生长的阶段;(3) 共生阶段,AMF菌丝进入到植物根系细胞内,并分化出根内菌丝和根外菌丝[
目前对菌根形态的鉴别多依赖于显微观察,难以对处于不同共生阶段的AMF组织进行大规模筛选。因此,目前对不同共生阶段AMF进行转录组测序和分析的研究极少,仅见Morin等(2019)对AMF共生阶段和非共生阶段的转录组进行的比较研究[
AMF的结构可大致分为根内和根外两部分。AMF根外部分主要包括孢子(spores)、芽管(germ tubes)、匍匐菌丝(runner hyphae)以及分枝状吸收结构(branched absorbing structures);其中孢子负责繁殖,芽管为孢子萌发初期形成的结构,匍匐菌丝主要负责养分运输,分枝状吸收结构主要负责土壤养分的吸收[
Kameoka等(2019)采用以SMART seq2方法构建RNA-seq文库的方式,对模式种异形根孢囊霉DAOM 197198不同菌根结构的转录本特征进行了研究,包括异形根孢囊霉的5种根外结构(成熟孢子、未成熟孢子、芽管、匍匐菌丝、分枝状吸收结构)和2种根内结构(根内菌丝和丛枝)[
AMF根内和根外菌根结构的基因表达也会受到寄主植物和土壤条件的影响。Bao等(2019)通过同位素示踪以及功能基因的表达特征分析研究了AMF与水稻的“养分交易”,发现淹水显著降低了AMF根内和根外结构的生物量;AMF向水稻的P供应量随着淹水强度的增加明显减少,且在水稻有较强养分需求的生理时期AMF供应的P要远高于其他发育时期[
通常认为,AMF对寄主植物的选择不具有明显的专一性。一种AMF能够同时侵染同种或不同种的寄主植物[
当AMF同时与2种及以上的寄主植物共生时,AMF转录本的差异首先体现在与养分交换及运输相关的基因上。Calabrese等(2019)研究了高P和低P条件下异形根孢囊霉BEG75接种对毛果杨和高粱转录组的影响[
AMF与不同寄主植物共生也涉及不同的信号交流过程,其中分泌蛋白被普遍认为是最有可能充当信号物质的对象。Zeng等(2018)发现,异形根孢囊霉在共生时期根内菌丝和丛枝中表达量更高的部分分泌蛋白含有核定位信号;他们通过荧光标记在寄主细胞中定位了该信号,证明了AMF的分泌蛋白能够与寄主细胞互作[
对于丛枝菌根这种广泛而重要的共生关系,以往的研究基本局限在寄主植物方面,而对于AMF方面的生理、分子层面的理解极为有限。尽管目前对于AMF转录组学的研究仍然偏少,但是已有的研究已经在较大程度上提高了对AMF不同共生结构、共生阶段以及与不同寄主相互作用等方面的理解。可以预见,伴随着测序技术的进步和AMF基因组学的发展,AMF转录组学的研究将在接下来的几年内迎来跨越式的发展。
AMF基因组和转录组的研究极大地加深了对AMF这类古老而重要微生物类群的理解。AMF基因组测序揭示了其基因组数量大、可变性高的特点;而缺乏植物细胞壁多糖降解酶以及脂肪酸合酶的相关基因验证了AMF严格共生生活方式的基因特点;此外,在AMF基因组中发现的有性生殖相关基因结构域为AMF的遗传方式提供了新的认识。AMF转录组研究初步揭示了不同的AMF结构、共生阶段以及应对不同类型寄主植物时AMF的转录本的差异,这种差异与不同条件下AMF的代谢特征是相适应的。以上在基因组和转录组层面开展的研究为深入理解AMF的生活特征、与寄主植物的互作方式以及对环境的适应性提供了重要参考。
近年来,基因组学和转录组学研究在高通量测序、多组学联用等技术推动下发展迅速。课题组成员前期结合宏基因组、宏转录组等研究手段深入解析了酸性矿山废水中细菌[
首先,AMF纯培养技术的革新。作为一种营专性共生的真菌,AMF目前仍无法实现真正意义上的纯培养,严重阻碍了AMF基因组和转录组的研究。最新研究通过脂肪酸的添加在一定程度上实现了纯培养,如何利用脂肪酸提高AMF的产孢率以及实现完全的纯培养将是值得重点关注的方向[
其次,AMF基因组中大量未知功能基因的解析。我们对AMF与寄主植物共生机制缺乏认识的一个重要原因在于大量AMF基因无法通过已有的基因组信息进行很好的注释,因此亟需结合实验手段和生物信息学技术对这些未知基因的功能进行挖掘和解析。基于分离培养和比较基因组学对不同种类的AMF进行研究为解决这一问题提供了思路[
再次,对非模式AMF类群的基因组和转录组的研究。目前已有的AMF测序工作主要集中在AMF的模式种异形根孢囊霉以及少数几个代表性AMF种类。后续应开展对目前所知甚少且演化上更为古老的原囊菌目和类球囊菌目中的AMF开展研究,以更全面地了解AMF类群的整体特征以及在不同分类水平上的基因组和转录组特征。
最后,AMF蛋白组层面的研究。目前关于AMF基因翻译水平的信息极为缺乏,已有的AMF蛋白质层面的信息都是通过对AMF基因组、转录组信息进行预测获得,而直接对AMF蛋白质的检测、分离和功能鉴定的研究几乎未见报道。鸟枪法蛋白质组学的发展或许能够为AMF蛋白组的研究提供新的方法[
感谢两位匿名审稿人为本文提出的建设性意见!
Brundrett MC, Tedersoo L. Evolutionary history of mycorrhizal symbioses and global host plant diversity.
Wang YT, Li YW, Li SS, Rosendahl S. Ignored diversity of arbuscular mycorrhizal fungi in co-occurring mycotrophic and non-mycotrophic plants.
Tedersoo L, Bahram M, Zobel M. How mycorrhizal associations drive plant population and community biology.
Wang B, Qiu YL. Phylogenetic distribution and evolution of mycorrhizas in land plants.
Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, Matasci N, Ayyampalayam S, Barker MS, Burleigh JG, Gitzendanner MA, Ruhfel BR, Wafula E, Der JP, Graham SW, Mathews S, Melkonian M, Soltis DE, Soltis PS, Miles NW, Rothfels CJ, Pokorny L, Shaw AJ, DeGironimo L, Stevenson DW, Surek B, Villarreal JC, Roure B, Philippe H, de Pamphilis CW, Chen T, Deyholos MK, Baucom RS, Kutchan TM, Augustin MM, Wang J, Zhang Y, Tian ZJ, Yan ZX, Wu XL, Sun X, Wong GKS, Leebens-Mack J. Phylotranscriptomic analysis of the origin and early diversification of land plants.
Compant S, van der Heijden MGA, Sessitsch A. Climate change effects on beneficial plant-microorganism interactions.
Li T, Hu YJ, Hao ZP, Li H, Wang YS, Chen BD. First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus
Garcia K, Doidy J, Zimmermann SD, Wipf D, Courty PE. Take a trip through the plant and fungal transportome of mycorrhiza.
Hu RY, Beguiristain T, Junet A, Leyval C. No significant transfer of the rare earth element samarium from spiked soil to alfalfa by
Bravo A, Brands M, Wewer V, Dörmann P, Harrison MJ. Arbuscular mycorrhiza-specific enzymes FatM and RAM2 fine-tune lipid biosynthesis to promote development of arbuscular mycorrhiza.
Jiang YN, Wang WX, Xie QJ, Liu N, Liu LX, Wang DP, Zhang XW, Yang C, Chen XY, Tang DZ, Wang ET. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi.
Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan GV, Breakspear A, Oldroyd GED, Eastmond PJ. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant.
Keymer A, Gutjahr C. Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond.
Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning.
van der Heijden MGA, Martin FM, Selosse MA, Sanders IR. Mycorrhizal ecology and evolution: the past, the present, and the future.
Kobae Y, Ohtomo R. An improved method for bright-field imaging of arbuscular mycorrhizal fungi in plant roots.
Liu F, Xu YJ, Han GM, Wang W, Li XY, Cheng BJ. Identification and functional characterization of a maize phosphate transporter induced by mycorrhiza formation.
Pel R, Dupin S, Schat H, Ellers J, Kiers ET, van Straalen NM. Growth benefits provided by different arbuscular mycorrhizal fungi to
Pauline CN, Ewen FK. Whole genome sequencing.
Land M, Hauser L, Jun SR, Nookaew I, Leuze MR, Ahn TH, Karpinets T, Lund O, Kora G, Wassenaar T, Poudel S, Ussery DW. Insights from 20 years of bacterial genome sequencing.
Chen LX, Méndez-García C, Dombrowski N, Servín-Garcidueñas LE, Eloe-Fadrosh EA, Fang BZ, Luo ZH, Tan S, Zhi XY, Hua ZS, Martinez-Romero E, Woyke T, Huang LN, Sánchez J, Peláez AI, Ferrer M, Baker BJ, Shu WS. Metabolic versatility of small Archaea Micrarchaeota and Parvarchaeota.
Tan S, Liu J, Fang Y, Hedlund BP, Lian ZH, Huang LY, Li JT, Huang LN, Li WJ, Jiang HC, Dong HL, Shu WS. Insights into ecological role of a new deltaproteobacterial order Candidatus Acidulodesulfobacterales by metagenomics and metatranscriptomics.
Chen MY, Teng WK, Zhao L, Hu CX, Zhou YK, Han BP, Song LR, Shu WS. Comparative genomics reveals insights into cyanobacterial evolution and habitat adaptation.
Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei Dit Frey N, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Ndikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, San Clemente H, Shapiro H, Van Tuinen D, Bécard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, Young JP, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis.
Jiang ZH, Zhou X, Li R, Michal JJ, Zhang SW, Dodson MV, Zhang ZW, Harland RM. Whole transcriptome analysis with sequencing: methods, challenges and potential solutions.
唐年武. 基于RNA-seq的丛枝菌根真菌Gigaspora rosea基因构成及其共生发育相关基因的分析. 华中农业大学博士学位论文, 2016.
Becquer A, Garcia K, Amenc L, Rivard C, Doré J, Trives-Segura C, Szponarski W, Russet S, Baeza Y, Lassalle-Kaiser B, Gay G, Zimmermann SD, Plassard C. The
Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, Canbäck B, Choi C, Cichocki N, Clum A, Colpaert J, Copeland A, Costa MD, Doré J, Floudas D, Gay G, Girlanda M, Henrissat B, Herrmann S, Hess J, Högberg N, Johansson T, Khouja HR, LaButti K, Lahrmann U, Levasseur A, Lindquist EA, Lipzen A, Marmeisse R, Martino E, Murat C, Ngan CY, Nehls U, Plett JM, Pringle A, Ohm RA, Perotto S, Peter M, Riley R, Rineau F, Ruytinx J, Salamov A, Shah F, Sun H, Tarkka M, Tritt A, Veneault-Fourrey C, Zuccaro A, Tunlid A, Grigoriev IV, Hibbett DS, Martin F. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists.
Ropars J, Toro KS, Noel J, Pelin A, Charron P, Farinelli L, Marton T, Krüger M, Fuchs J, Brachmann A, Corradi N. Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi.
Chen ECH, Morin E, Beaudet D, Noel J, Yildirir G, Ndikumana S, Charron P, St-Onge C, Giorgi J, Krüger M, Marton T, Ropars J, Grigoriev IV, Hainaut M, Henrissat B, Roux C, Martin F, Corradi N. High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont
Morin E, Miyauchi S, San Clemente H, Chen ECH, Pelin A, De La Providencia I, Ndikumana S, Beaudet D, Hainaut M, Drula E, Kuo A, Tang N, Roy S, Viala J, Henrissat B, Grigoriev IV, Corradi N, Roux C, Martin FM. Comparative genomics of
Sugiura Y, Akiyama R, Tanaka S, Yano K, Kameoka H, Marui S, Saito M, Kawaguchi M, Akiyama K, Saito K. Myristate can be used as a carbon and energy source for the asymbiotic growth of arbuscular mycorrhizal fungi.
Kameoka H, Tsutsui I, Saito K, Kikuchi Y, Handa Y, Ezawa T, Hayashi H, Kawaguchi M, Akiyama K. Stimulation of asymbiotic sporulation in arbuscular mycorrhizal fungi by fatty acids.
Kobayashi Y, Maeda T, Yamaguchi K, Kameoka H, Tanaka S, Ezawa T, Shigenobu S, Kawaguchi M. The genome of
Lanfranco L, Young JPW. Genetic and genomic glimpses of the elusive arbuscular mycorrhizal fungi.
Kokkoris V, Chagnon PL, Yildirir G, Clarke K, Goh D, MacLean AM, Dettman J, Stefani F, Corradi N. Host identity influences nuclear dynamics in arbuscular mycorrhizal fungi.
Martin F, Gianinazzi-Pearson V, Hijri M, Lammers P, Requena N, Sanders IR, Shachar-Hill Y, Shapiro H, Tuskan GA, Young JPW. The long hard road to a completed
Barman J, Samanta A, Saha B, Datta S. Mycorrhiza.
Parniske M.
Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C. An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (
Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O'Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE. A Phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data.
Bonfante P, Venice F.
Bruns TD, Corradi N, Redecker D, Taylor JW, Öpik M.
Sanders IR. Sex, plasticity, and biologically significant variation in one
Gosling P, Proctor M, Jones J, Bending GD. Distribution and diversity of
Bills RJ, Morton JB. A combination of morphology and 28S rRNA gene sequences provide grouping and ranking criteria to merge eight into three
Miyauchi S, Kiss E, Kuo A, Drula E, Kohler A, Sánchez-García M, Morin E, Andreopoulos B, Barry KW, Bonito G, Buée M, Carver A, Chen C, Cichocki N, Clum A, Culley D, Crous PW, Fauchery L, Girlanda M, Hayes RD, Kéri Z, LaButti K, Lipzen A, Lombard V, Magnuson J, Maillard F, Murat C, Nolan M, Ohm RA, Pangilinan J, de Freitas Pereira M, Perotto S, Peter M, Pfister S, Riley R, Sitrit Y, Benjamin Stielow J, Szöllősi G, Žifčáková L, Štursová M, Spatafora JW, Tedersoo L, Vaario LM, Yamada A, Yan M, Wang PF, Xu JP, Bruns T, Baldrian P, Vilgalys R, Dunand C, Henrissat B, Grigoriev IV, Hibbett D, Nagy LG, Martin FM. Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits.
Holland PWH, Marlétaz F, Maeso I, Dunwell TL, Paps J. New genes from old: asymmetric divergence of gene duplicates and the evolution of development.
Angelard C, Tanner CJ, Fontanillas P, Niculita-Hirzel H, Masclaux F, Sanders IR. Rapid genotypic change and plasticity in arbuscular mycorrhizal fungi is caused by a host shift and enhanced by segregation.
Sędzielewska KA, Fuchs J, Temsch EM, Baronian K, Watzke R, Kunze G. Estimation of the
Chen EC, Mathieu S, Hoffrichter A, Sedzielewska-Toro K, Peart M, Pelin A, Ndikumana S, Ropars J, Dreissig S, Fuchs J, Brachmann A, Corradi N. Single nucleus sequencing reveals evidence of inter-nucleus recombination in arbuscular mycorrhizal fungi.
Tang NW, San Clemente H, Roy S, Bécard G, Zhao B, Roux C. A survey of the gene repertoire of
Malbreil M, Tisserant E, Martin F, Roux C. Genomics of arbuscular mycorrhizal fungi. Advances in Botanical Research. Amsterdam: Elsevier, 2014: 259-290.
Feschotte C, Jiang N, Wessler SR. Plant transposable elements: where genetics meets genomics.
Murphy TR, Xiao R, Hamilton-Brehm SD. Hybrid genome de novo assembly with methylome analysis of the anaerobic thermophilic subsurface bacterium
Malinovsky FG, Fangel JU, Willats WGT. The role of the cell wall in plant immunity.
Chen M, Bruisson S, Bapaume L, Darbon G, Glauser G, Schorderet M, Reinhardt D. VAPYRIN attenuates defence by repressing PR gene induction and localized lignin accumulation during arbuscular mycorrhizal symbiosis of
Bago B, Pfeffer PE, Abubaker J, Jun J, Allen JW, Brouillette J, Douds DD, Lammers PJ, Shachar-Hill Y. Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid.
Teichmann B, Linne U, Hewald S, Marahiel MA, Bölker M. A biosynthetic gene cluster for a secreted cellobiose lipid with antifungal activity from
Wewer V, Brands M, Dörmann P. Fatty acid synthesis and lipid metabolism in the obligate biotrophic fungus
Trépanier M, Bécard G, Moutoglis P, Willemot C, Gagné S, Avis TJ, Rioux JA. Dependence of arbuscular-mycorrhizal fungi on their plant host for palmitic acid synthesis.
Vangelisti A, Turrini A, Sbrana C, Avio L, Giordani T, Natali L, Giovannetti M, Cavallini A. Gene expression in
Halary S, Malik SB, Lildhar L, Slamovits CH, Hijri M, Corradi N. Conserved meiotic machinery in
Riley R, Corradi N. Searching for clues of sexual reproduction in the genomes of arbuscular mycorrhizal fungi.
Riley R, Charron P, Idnurm A, Farinelli L, Dalpé Y, Martin F, Corradi N. Extreme diversification of the mating type-high-mobility group (
Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, Da Silva C, Gomez SK, Koul R, Ferrol N, Fiorilli V, Formey D, Franken P, Helber N, Hijri M, Lanfranco L, Lindquist E, Liu Y, Malbreil M, Morin E, Poulain J, Shapiro H, van Tuinen D, Waschke A, Azcón-Aguilar C, Bécard G, Bonfante P, Harrison MJ, Küster H, Lammers P, Paszkowski U, Requena N, Rensing SA, Roux C, Sanders IR, Shachar-Hill Y, Tuskan G, Young JPW, Gianinazzi-Pearson V, Martin F. The transcriptome of the arbuscular mycorrhizal fungus
Bunn RA, Simpson DT, Bullington LS, Lekberg Y, Janos DP. Revisiting the 'direct mineral cycling' hypothesis: arbuscular mycorrhizal fungi colonize leaf litter, but why?
Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N. A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus
Zhang L, Feng G, Declerck S. Signal beyond nutrient, fructose, exuded by an arbuscular mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium.
Wang XX, Hoffland E, Feng G, Kuyper TW. Phosphate uptake from phytate due to hyphae-mediated phytase activity by arbuscular mycorrhizal maize.
Sun XP, Chen WB, Ivanov S, MacLean AM, Wight H, Ramaraj T, Mudge J, Harrison MJ, Fei ZJ. Genome and evolution of the arbuscular mycorrhizal fungus
Venice F, Ghignone S, Salvioli di Fossalunga A, Amselem J, Novero M, Xie XN, Sędzielewska Toro K, Morin E, Lipzen A, Grigoriev IV, Henrissat B, Martin FM, Bonfante P. At the
Uehling J, Gryganskyi A, Hameed K, Tschaplinski T, Misztal PK, Wu S, Desirò A, Vande Pol N, Du Z, Zienkiewicz A, Zienkiewicz K, Morin E, Tisserant E, Splivallo R, Hainaut M, Henrissat B, Ohm R, Kuo A, Yan J, Lipzen A, Nolan M, LaButti K, Barry K, Goldstein AH, Labbé J, Schadt C, Tuskan G, Grigoriev I, Martin F, Vilgalys R, Bonito G. Comparative genomics of
Wang L, Chen W, Feng Y, Ren Y, Gu ZN, Chen HQ, Wang HC, Thomas MJ, Zhang BX, Berquin IM, Li Y, Wu JS, Zhang HX, Song YD, Liu X, Norris JS, Wang S, Du P, Shen JG, Wang N, Yang YL, Wang W, Feng L, Ratledge C, Zhang H, Chen YQ. Genome characterization of the oleaginous fungus
Corrochano LM, Kuo A, Marcet-Houben M, Polaino S, Salamov A, Villalobos-Escobedo JM, Grimwood J, Álvarez MI, Avalos J, Bauer D, Benito EP, Benoit I, Burger G, Camino LP, Cánovas D, Cerdá-Olmedo E, Cheng JF, Domínguez A, Eliáš M, Eslava AP, Glaser F, Gutiérrez G, Heitman J, Henrissat B, Iturriaga EA, Lang BF, Lavín JL, Lee SC, Li WJ, Lindquist E, López-García S, Luque EM, Marcos AT, Martin J, McCluskey K, Medina HR, Miralles-Durán A, Miyazaki A, Muñoz-Torres E, Oguiza JA, Ohm RA, Olmedo M, Orejas M, Ortiz-Castellanos L, Pisabarro AG, Rodríguez-Romero J, Ruiz-Herrera J, Ruiz-Vázquez R, Sanz C, Schackwitz W, Shahriari M, Shelest E, Silva-Franco F, Soanes D, Syed K, Tagua VG, Talbot NJ, Thon MR, Tice H, de Vries RP, Wiebenga A, Yadav JS, Braun EL, Baker SE, Garre V, Schmutz J, Horwitz BA, Torres-Martínez S, Idnurm A, Herrera-Estrella A, Gabaldón T, Grigoriev IV. Expansion of signal transduction pathways in fungi by extensive genome duplication.
Tsuzuki S, Handa Y, Takeda N, Kawaguchi M. Strigolactone-induced putative secreted protein 1 is required for the establishment of symbiosis by the arbuscular mycorrhizal fungus
Ruzicka D, Chamala S, Barrios-Masias FH, Martin F, Smith S, Jackson LE, Barbazuk WB, Schachtman DP. Inside arbuscular mycorrhizal roots-molecular probes to understand the symbiosis.
Kameoka H, Maeda T, Okuma N, Kawaguchi M. Structure-specific regulation of nutrient transport and metabolism in arbuscular mycorrhizal fungi.
Garcia K, Delaux PM, Cope KR, Ané JM. Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses.
Zeng T, Holmer R, Hontelez J, te Lintel-Hekkert B, Marufu L, de Zeeuw T, Wu FY, Schijlen E, Bisseling T, Limpens E. Host- and stage-dependent secretome of the arbuscular mycorrhizal fungus
Schweiger R, Baier MC, Müller C. Arbuscular mycorrhiza-induced shifts in foliar metabolism and photosynthesis mirror the developmental stage of the symbiosis and are only partly driven by improved phosphate uptake.
Bago B, Azcón-Aguilar C, Piché Y. Architecture and developmental dynamics of the external mycelium of the arbuscular mycorrhizal fungus
Tian CJ, Kasiborski B, Koul R, Lammers PJ, Bücking H, Shachar-Hill Y. Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux.
Bao XZ, Wang YT, Olsson PA. Arbuscular mycorrhiza under water-Carbon-phosphorus exchange between rice and arbuscular mycorrhizal fungi under different flooding regimes.
Calabrese S, Cusant L, Sarazin A, Niehl A, Erban A, Brulé D, Recorbet G, Wipf D, Roux C, Kopka J, Boller T, Courty PE. Imbalanced regulation of fungal nutrient transports according to phosphate availability in a symbiocosm formed by poplar,
Beaudet D, Chen ECH, Mathieu S, Yildirir G, Ndikumana S, Dalpé Y, Séguin S, Farinelli L, Stajich JE, Corradi N. Ultra-low input transcriptomics reveal the spore functional content and phylogenetic affiliations of poorly studied arbuscular mycorrhizal fungi.
Salvioli A, Ghignone S, Novero M, Navazio L, Venice F, Bagnaresi P, Bonfante P. Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential.
Kuang JL, Huang LN, He ZL, Chen LX, Hua ZS, Jia P, Li SJ, Liu J, Li JT, Zhou JZ, Shu WS. Predicting taxonomic and functional structure of microbial communities in acid mine drainage.
Recorbet G, Courty PE, Wipf D. Recovery of extra-radical fungal peptides amenable for shotgun protein profiling in arbuscular mycorrhizae.