期刊论文详细信息
Genome Biology
Analyzing the soybean transcriptome during autoregulation of mycorrhization identifies the transcription factors GmNF-YA1a/b as positive regulators of arbuscular mycorrhization
Bettina Hause2  Peter M Gresshoff1  Sara Schaarschmidt3 
[1] ARC Centre of Excellence for Integrative Legume Research (CILR), The University of Queensland, St. Lucia, Queensland 4072, Australia;Leibniz Institute of Plant Biochemistry (IPB), Weinberg 3, 06120 Halle (Saale), Germany;Humboldt-Universität zu Berlin, Faculty of Agriculture and Horticulture, Division Urban Plant Ecophysiology, Lentzeallee 55-57, 14195 Berlin, Germany
关键词: split-root system;    quantitative RT-PCR;    Glycine max (soybean);    Rhizophagus irregularis;    CCAAT-binding transcription factor NF-Y;    arbuscular mycorrhiza;    autoregulation;    GeneChip;    Affymetrix annexin;   
Others  :  865368
DOI  :  10.1186/gb-2013-14-6-r62
 received in 2013-02-26, accepted in 2013-06-18,  发布年份 2013
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【 摘 要 】

Background

Similarly to the legume-rhizobia symbiosis, the arbuscular mycorrhiza interaction is controlled by autoregulation representing a feedback inhibition involving the CLAVATA1-like receptor kinase NARK in shoots. However, little is known about signals and targets down-stream of NARK. To find NARK-related transcriptional changes in mycorrhizal soybean (Glycine max) plants, we analyzed wild-type and two nark mutant lines interacting with the arbuscular mycorrhiza fungus Rhizophagus irregularis.

Results

Affymetrix GeneChip analysis of non-inoculated and partially inoculated plants in a split-root system identified genes with potential regulation by arbuscular mycorrhiza or NARK. Most transcriptional changes occur locally during arbuscular mycorrhiza symbiosis and independently of NARK. RT-qPCR analysis verified nine genes as NARK-dependently regulated. Most of them have lower expression in roots or shoots of wild type compared to nark mutants, including genes encoding the receptor kinase GmSIK1, proteins with putative function as ornithine acetyl transferase, and a DEAD box RNA helicase. A predicted annexin named GmAnnx1a is differentially regulated by NARK and arbuscular mycorrhiza in distinct plant organs. Two putative CCAAT-binding transcription factor genes named GmNF-YA1a and GmNF-YA1b are down-regulated NARK-dependently in non-infected roots of mycorrhizal wild-type plants and functional gene analysis confirmed a positive role for these genes in the development of an arbuscular mycorrhiza symbiosis.

Conclusions

Our results indicate GmNF-YA1a/b as positive regulators in arbuscular mycorrhiza establishment, whose expression is down-regulated by NARK in the autoregulated root tissue thereby diminishing subsequent infections. Genes regulated independently of arbuscular mycorrhization by NARK support an additional function of NARK in symbioses-independent mechanisms.

【 授权许可】

   
2013 Schaarschmidt et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Schüßler A, Schwarzott D, Walker C: A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 2001, 105:1413-1421.
  • [2]Brundrett MC: Coevolution of roots and mycorrhizas of land plants. New Phytol 2002, 154:275-304.
  • [3]Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H: Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 2011, 333:880-882.
  • [4]van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR: Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 1998, 396:69-72.
  • [5]Smith FA, Smith SE: Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol 1997, 137:373-388.
  • [6]Kereszt A, Kondorosi E: Unlocking the door to invasion. Science 2011, 331:865-866.
  • [7]Markmann K, Parniske M: Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci 2009, 14:77-86.
  • [8]Oldroyd GED, Harrison MJ, Paszkowski U: Reprogramming plant cells for endosymbiosis. Science 2009, 324:753-754.
  • [9]Streng A, op den Camp R, Bisseling T, Geurts R: Evolutionary origin of rhizobium Nod factor signaling. Plant Signal Behav 2011, 6:1510-1514.
  • [10]Gough C, Cullimore J: Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol Plant Microbe Interact 2011, 24:867-878.
  • [11]Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Becard G, Denarie J: Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 2011, 469:58-63.
  • [12]Ferguson BJ, Indrasumunar A, Hayashi S, Lin M-H, Lin Y-H, Reid DE, Gresshoff PM: Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 2010, 52:61-76.
  • [13]Hause B, Schaarschmidt S: The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry 2009, 70:1589-1599.
  • [14]Mortier V, Holsters M, Goormachtig S: Never too many? How legumes control nodule numbers. Plant Cell Environ 2012, 35:245-258.
  • [15]Reid DE, Ferguson BJ, Hayashi S, Lin Y-H, Gresshoff PM: Molecular mechanisms controlling legume autoregulation of nodulation. Ann Bot 2011, 108:789-795.
  • [16]Staehelin C, Xie Z-P, Illana A, Vierheilig H: Long-distance transport of signals during symbiosis. Are nodule formation and mycorrhization autoregulated in a similar way? Plant Signal Behav 2011, 6:372-377.
  • [17]Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM: Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 2003, 299:109-112.
  • [18]Caetano-Anolles G, Gresshoff PM: Early induction of feedback regulatory responses governing nodulation in soybean. Plant Sci 1990, 71:69.
  • [19]Delves AC, Mathews A, Day DA, Carter AS, Carroll BJ, Gresshoff PM: Regulation of the soybean-rhizobium nodule symbiosis by shoot and root factors. Plant Physiol 1986, 82:588-590.
  • [20]Carroll BJ, McNeil DL, Gresshoff PM: A supernodulation and nitrate-tolerant symbiotic (nts) soybean mutant. Plant Physiol 1985, 78:34-40.
  • [21]Lin M-H, Gresshoff PM, Ferguson BJ: Systemic regulation of soybean nodulation by acidic growth conditions. Plant Physiol 2012, 160:2028-2039.
  • [22]Meixner C, Ludwig-Mueller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H: Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 2005, 222:709-715.
  • [23]Sakamoto K, Nohara Y: Soybean (Glycine max [L.] Merr.) shoots systemically control arbuscule formation in mycorrhizal symbiosis. Soil Sci Plant Nutr 2009, 55:252-257.
  • [24]Shrihari PC, Sakamoto K, Inubushi K, Akao S: Interaction between supernodulating or non-nodulating mutants of soybean and two arbuscular mycorrhizal fungi. Mycorrhiza 2000, 10:101-106.
  • [25]Solaiman MZ, Senoo K, Kawaguchi M, Imaizumi-Anraku H, Akao S, Tanaka A, Obata H: Characterization of mycorrhizas formed by Glomus sp. on roots of hypernodulating mutants of Lotus japonicus. J Plant Res 2000, 113:443-448.
  • [26]Pearson JN, Abbott LK, Jasper DA: Mediation of competition between two colonizing VA mycorrhizal fungi by the host plant. New Phytol 1993, 123:93-98.
  • [27]Vierheilig H, Garcia-Garrido JM, Wyss U, Piché Y: Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biol Biochem 2000, 32:589-595.
  • [28]Catford J-G, Staehelin C, Lerat S, Piche Y, Vierheilig H: Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors. J Exp Bot 2003, 54:1481-1487.
  • [29]Kenjo T, Yamaya H, Arima Y: Shoot-synthesized nodulation-restricting substances of wild-type soybean present in two different high-performance liquid chromatography peaks of the ethanol-soluble medium-polarity fraction. Soil Sci Plant Nutr 2010, 56:399-406.
  • [30]Lin Y-H, Ferguson BJ, Kereszt A, Gresshoff PM: Suppression of hypernodulation in soybean by a leaf-extracted, NARK- and Nod factor-dependent, low molecular mass fraction. New Phytol 2010, 185:1074-1086.
  • [31]Magori S, Oka-Kira E, Shibata S, Umehara Y, Kouchi H, Hase Y, Tanaka A, Sato S, Tabata S, Kawaguchi M: TOO MUCH LOVE, a root regulator associated with the long-distance control of nodulation in Lotus japonicus. Mol Plant Microbe Interact 2009, 22:259-268.
  • [32]Kinkema M, Gresshoff PM: Investigation of downstream signals of the soybean autoregulation of nodulation receptor kinase GmNARK. Mol Plant Microbe Interact 2008, 21:1337-1348.
  • [33]Seo HS, Li J, Lee S-Y, Yu J-W, Kim K-H, Lee S-H, Lee I-J, Paek N-C: The hypernodulating nts mutation induces jasmonate synthetic pathway in soybean leaves. Mol Cells 2007, 24:185-193.
  • [34]van Noorden GE, Ross JJ, Reid JB, Rolfe BG, Mathesius U: Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant. Plant Physiol 2006, 140:1494-1506.
  • [35]Reid DE, Hayashi S, Lorenc M, Stiller J, Edwards D, Gresshoff PM, Ferguson BJ: Identification of systemic responses in soybean nodulation by xylem sap feeding and complete transcriptome sequencing reveal a novel component of the autoregulation pathway. Plant Biotechnol J 2012, 10:680-689.
  • [36]Meixner C, Vegvarib G, Ludwig-Müller J, Gagnond H, Steinkellner S, Staehelin C, Gresshoff P, Vierheilig H: Two defined alleles of the LRR receptor kinase GmNARK in supernodulating soybean govern differing autoregulation of mycorrhization. Physiol Plant 2007, 130:261-270.
  • [37]Bucher P: Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol 1990, 212:563-578.
  • [38]Dolfini D, Gatta R, Mantovani R: NF-Y and the transcriptional activation of CCAAT promoters. Crit Rev Biochem Mol Biol 2012, 47:29-49.
  • [39]Edwards D, Murray JAH, Smith AG: Multiple genes encoding the conserved CCAAT-box transcription factor complex are expressed in Arabidopsis. Plant Physiol 1998, 117:1015-1022.
  • [40]Mantovani R: The molecular biology of the CCAAT-binding factor NF-Y. Gene 1999, 239:15-27.
  • [41]Laloum T, De Mita S, Gamas P, Baudin M, Niebel A: CCAAT-box binding transcription factors in plants: Y so many? Trends Plant Sci 2012., 1001NO of Pages 10
  • [42]Petroni K, Kumimoto RW, Gnesutta N, Calvenzani V, Fornari M, Tonelli C, Holt BF, Mantovani R: The promiscuous life of plant NUCLEAR FACTOR Y transcription factors. Plant Cell Online 2012, 24:4777-4792.
  • [43]Asamizu E, Shimoda Y, Kouchi H, Tabata S, Sato S: A positive regulatory role for LjERF1 in the nodulation process is revealed by systematic analysis of nodule-associated transcription factors of Lotus japonicus. Plant Physiol 2008, 147:2030-2040.
  • [44]Combier JP, de Billy F, Gamas P, Niebel A, Rivas S: Trans-regulation of the expression of the transcription factor MtHAP2-1 by a uORF controls root nodule development. Genes Dev 2008, 22:1549-1559.
  • [45]Combier J-P, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernié T, Ott T, Gamas P, Crespi M, Niebel A: MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 2006, 20:3084-3088.
  • [46]El Yahyaoui F, Küster H, Ben Amor B, Hohnjec N, Pühler A, Becker A, Gouzy J, Vernie T, Gough C, Niebel A, Godiard L, Gamas P: Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol 2004, 136:3159-3176.
  • [47]Hayashi S, Reid DE, Lorenc MT, Stiller J, Edwards D, Gresshoff PM, Ferguson BJ: Transient Nod factor-dependent gene expression in the nodulation-competent zone of soybean (Glycine max [L.] Merr.) roots. Plant Biotechnol J 2012, 10:995-1010.
  • [48]Hogekamp C, Arndt D, Pereira PA, Becker JD, Hohnjec N, Küster H: Laser microdissection unravels cell-type-specific transcription in arbuscular mycorrhizal roots, including CAAT-box transcription factor gene expression correlating with fungal contact and spread. Plant Physiol 2011, 157:2023-2043.
  • [49]Libault M, Joshi T, Takahashi K, Hurley-Sommer A, Puricelli K, Blake S, Finger RE, Taylor CG, Xu D, Nguyen HT, Stacey G: Large-scale analysis of putative soybean regulatory gene expression identifies a Myb gene involved in soybean nodule development. Plant Physiol 2009, 151:1207-1220.
  • [50]Meschini EP, Blanco FA, Zanetti ME, Beker MP, Küster H, Pühler A, Aguilar OM: Host genes involved in nodulation preference in common bean (Phaseolus vulgaris)-Rhizobium etli symbiosis revealed by suppressive subtractive hybridization. Mol Plant Microbe Interact 2008, 21:459-468.
  • [51]Moreau S, Verdenaud M, Ott T, Letort S, de Billy F, Niebel A, Gouzy J, de Carvalho-Niebel F, Gamas P: Transcription reprogramming during root nodule development in Medicago truncatula. PLoS ONE 2011, 6:e16463.
  • [52]Soyano T, Kouchi H, Hirota A, Hayashi M: NODULE INCEPTION directly targets NF-Y subunit genes to regulate essential processes of root nodule development in Lotus japonicus. PLoS Genet 2013, 9:e1003352.
  • [53]Zanetti ME, Blanco FA, Beker MP, Battaglia M, Aguilar OM: A C subunit of the plant nuclear factor NF-Y required for rhizobial infection and nodule development affects partner selection in the common bean-Rhizobium etli symbiosis. Plant Cell Online 2010, 22:4142-4157.
  • [54]Vierheilig H: Further root colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after a critical level of root colonization. J Plant Physiol 2004, 161:339-341.
  • [55]Corradi N, Kuhn G, Sanders IR: Monophyly of β-tubulin and H+-ATPase gene variants in Glomus intraradices: consequences for molecular evolutionary studies of AM fungal genes. Fungal Genet Biol 2004, 41:262-273.
  • [56]Floß DS, Hause B, Lange PR, Küster H, Strack D, Walter MH: Knock-down of the MEP pathway isogene 1-deoxy-d-xylulose 5-phosphate synthase 2 inhibits formation of arbuscular mycorrhiza-induced apocarotenoids, and abolishes normal expression of mycorrhiza-specific plant marker genes. Plant J 2008, 56:86-100.
  • [57]Li C, Wong WH: Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proc Natl Acad Sci USA 2001, 98:31-36.
  • [58]Hohnjec N, Vieweg MF, Puhler A, Becker A, Kuster H: Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 2005, 137:1283-1301.
  • [59]Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Pühler A, Perlick AM, Küster H: Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Mol Plant Microbe Interact 2004, 17:1063-1077.
  • [60]Wulf A, Manthey K, Doll J, Perlick AM, Linke B, Bekel T, Meyer F, Franken P, Kuster H, Krajinski F: Transcriptional changes in response to arbuscular mycorrhiza development in the model plant Medicago truncatula. Mol Plant Microbe Interact 2003, 16:306-314.
  • [61]Guether M, Balestrini R, Hannah M, He J, Udvardi MK, Bonfante P: Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol 2009, 182:200-212.
  • [62]Liu J, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ: Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell Online 2003, 15:2106-2123.
  • [63]Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ: Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 2007, 50:529-544.
  • [64]Güimil S, Chang H-S, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U: Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci USA 2005, 102:8066-8070.
  • [65]Frickey T, Weiller G: Analyzing microarray data using CLANS. Bioinformatics 2007, 23:1170-1171.
  • [66]Terakado J, Yoneyama T, Fujihara S: Shoot-applied polyamines suppress nodule formation in soybean (Glycine max). J Plant Physiol 2006, 163:497-505.
  • [67]Adio AM, Casteel CL, De Vos M, Kim JH, Joshi V, Li B, Juéry C, Daron J, Kliebenstein DJ, Jander G: Biosynthesis and defensive function of Nδ-acetylornithine, a jasmonate-induced Arabidopsis metabolite. Plant Cell Online 2011, 23:3303-3318.
  • [68]Kalamaki MS, Georgios Merkouropoulos , Kanellis AK: Can ornithine accumulation modulate abiotic stress tolerance in Arabidopsis? Plant Signal Behav 2009, 4:1099-1101.
  • [69]Takahashi T, Kakehi J-I: Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 2010, 105:1-6.
  • [70]Cordin O, Banroques J, Tanner NK, Linder P: The DEAD-box protein family of RNA helicases. Gene 2006, 367:17-37.
  • [71]Gong Z, Dong C-H, Lee H, Zhu J, Xiong L, Gong D, Stevenson B, Zhub J-K: A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 2005, 17:256-267.
  • [72]Schnabel E, Journet E-P, Carvalho-Niebel F, Duc G, Frugoli J: The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol 2005, 58:809-822.
  • [73]Wopereis J, Pajuelo E, Dazzo FB, Jiang Q, Gresshoff PM, Bruijn FJd, Stougaard J, Szczyglowski K: Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J 2000, 23:97-114.
  • [74]Konopka-Postupolska D, Clark G, Hofmann A: Structure, function and membrane interactions of plant annexins: An update. Plant Sci 2011, 181:230-241.
  • [75]Talukdar T, Gorecka K, de Carvalho-Niebel F, Downie J, Cullimore J, Pikula S: Annexins-calcium- and membrane-binding proteins in the plant kingdom: potential role in nodulation and mycorrhization in Medicago truncatula. Acta Biochim Pol 2009, 56:199-210.
  • [76]Amiour N, Recorbet G, Robert F, Gianinazzi S, Dumas-Gaudot E: Mutations in DMI3 and SUNN modify the appressorium-responsive root proteome in arbuscular mycorrhiza. Mol Plant Microbe Interact 2006, 19:988-997.
  • [77]de Carvalho-Niebel F, Timmers ACJ, Chabaud M, Defaux-Petras A, Barker DG: The Nod factor-elicited annexin MtAnn1 is preferentially localised at the nuclear periphery in symbiotically activated root tissues of Medicago truncatula. Plant J 2002, 32:343-352.
  • [78]Benning UF, Tamot B, Guelette BS, Hoffmann-Benning S: New aspects of phloem-mediated long-distance lipid signaling in plants. Front Plant Sci 2012, 3:53.
  • [79]Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, et al.: Genome sequence of the palaeopolyploid soybean. Nature 2010, 463:178-183.
  • [80]SoyDB. [http://planttfdb.cbi.edu.cn/index.php?sp=Gma] webcite
  • [81]Wang Z, Libault M, Joshi T, Valliyodan B, Nguyen H, Xu D, Stacey G, Cheng J: SoyDB: a knowledge database of soybean transcription factors. BMC Plant Biol 2010, 10:14. BioMed Central Full Text
  • [82]'Gene Networks in Seed Development' Soybean IVT Array Annotation. [http://www.seedgenenetwork.net/annotate] webcite
  • [83]Harrison M, Dewbre G, Liu J: A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 2002, 14:2413-2429.
  • [84]Javot H, Penmetsa R, Terzaghi N, Cook D, Harrison M: A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 2007, 30:1720-1725.
  • [85]Qin L, Zhao J, Tian J, Chen L, Sun Z, Guo Y, Lu X, Gu M, Xu G, Liao H: The high-affinity phosphate transporter GmPT5 regulates phosphate transport to nodules and nodulation in soybean. Plant Physiol 2012, 159:1634-1643.
  • [86]Tamura Y, Kobae Y, Mizuno T, Hata S: Identification and expression analysis of arbuscular mycorrhiza-inducible phosphate transporter genes of soybean. Biosci Biotechnol Biochem 2012, 76:309-313.
  • [87]Catford J, Staehelin C, Larose G, Piché Y, Vierheilig H: Systemically suppressed isoflavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant Soil 2006, 285:257-266.
  • [88]Hewitt EJ: Sand and water culture methods used in the study of plant nutrition. Farnhan Royal: Commonwealth Agricultural Bureaux; 1966.
  • [89]Schüßler A, Walker C: The Glomeromycota. A species list with new families and new genera. Arthur Schüßler & Christopher Walker, Gloucester. Published in December 2010 in libraries at The Royal Botanic Garden Edinburgh, The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University; 2010.
  • [90]Maier W, Peipp H, Schmidt J, Wray V, Strack D: Levels of a terpenoid glycoside (blumenin) and cell wall-bound phenolics in some cereal mycorrhizas. Plant Physiol 1995, 109:465-470.
  • [91]Limpens E, Ramos J, Franken C, Raz V, Compaan B, Franssen H, Bisseling T, Geurts R: RNA interference in Agrobacterium rhizogenes-transformed roots of Arabidopsis and Medicago truncatula. J Exp Bot 2004, 55:983-992.
  • [92]Kereszt A, Li D, Indrasumunar A, Nguyen CDT, Nontachaiyapoom S, Kinkema M, Gresshoff PM: Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nat Protoc 2007, 2:948-952.
  • [93]Vierheilig H, Coughlan AP, Wyss U, Piché Y: Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 1998, 64:5004-5007.
  • [94]NCBI BLAST. [http://blast.ncbi.nlm.nih.gov/Blast.cgi] webcite
  • [95]Phytozome. [http://www.phytozome.net] webcite
  • [96]Dash S, Van Hemert J, Hong L, Wise RP, Dickerson JA: PLEXdb: gene expression resources for plants and plant pathogens. Nucleic Acids Res 2012, 40:D1194-D1201.
  • [97]PLEXdb Experiment GM53. [http:/ / www.plexdb.org/ modules/ PD_browse/ experiment_browser.php?experiment=G M53] webcite
  • [98]Edgar R, Domrachev M, Lash AE: Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210.
  • [99]GEO Series GSE44685. [http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE44685] webcite
  • [100]Schmittgen TD, Livak KJ: Analyzing real-time PCR data by the comparative CT method. Nat Protoc 2008, 3:1101-1108.
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