BMC Genomics | |
An RNA-Seq based gene expression atlas of the common bean | |
Carroll P Vance3  Georgina Hernandez2  Patrick X Zhao7  Xinbin Dai7  Jun Li7  Philip E McClean6  Scott A Jackson4  Susan S Miller1  Bruna Bucciarelli1  Fengli Fu3  Luis P Iniguez2  Jamie A O’Rourke5  | |
[1] USDA-Agricultural Research Service, Plant Science Research Unit, St. Paul, MN 55108, USA;Centro de Ciencias Genomicas, Universidad Nacional Autonoma de Mexico, 66210 Cuernavaca, Mor, Mexico;Department of Agronomy and Plant Genetics, University of Minnesota, St. Paul, MN 55108, USA;Center for Applied Genetic Technologies, University of Georgia, Athens, GA 30602, USA;Current Address: USDA-ARS, Corn Insect Crop Genetics Research Unit, Iowa State University, Ames, IA 50011, USA;Department of Plant Sciences, North Dakota State University, Fargo, ND 58105, USA;Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, OK 73401, USA | |
关键词: SRP046307; Expression atlas; Symbiotic nitrogen fixation; RNA-Seq; Common bean; Phaseolus vulgaris cv Negro jamapa; | |
Others : 1136271 DOI : 10.1186/1471-2164-15-866 |
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received in 2014-05-08, accepted in 2014-09-24, 发布年份 2014 | |
【 摘 要 】
Background
Common bean (Phaseolus vulgaris) is grown throughout the world and comprises roughly 50% of the grain legumes consumed worldwide. Despite this, genetic resources for common beans have been lacking. Next generation sequencing, has facilitated our investigation of the gene expression profiles associated with biologically important traits in common bean. An increased understanding of gene expression in common bean will improve our understanding of gene expression patterns in other legume species.
Results
Combining recently developed genomic resources for Phaseolus vulgaris, including predicted gene calls, with RNA-Seq technology, we measured the gene expression patterns from 24 samples collected from seven tissues at developmentally important stages and from three nitrogen treatments. Gene expression patterns throughout the plant were analyzed to better understand changes due to nodulation, seed development, and nitrogen utilization. We have identified 11,010 genes differentially expressed with a fold change ≥ 2 and a P-value < 0.05 between different tissues at the same time point, 15,752 genes differentially expressed within a tissue due to changes in development, and 2,315 genes expressed only in a single tissue. These analyses identified 2,970 genes with expression patterns that appear to be directly dependent on the source of available nitrogen. Finally, we have assembled this data in a publicly available database, The Phaseolus vulgaris Gene Expression Atlas (Pv GEA), http://plantgrn.noble.org/PvGEA/ webcite . Using the website, researchers can query gene expression profiles of their gene of interest, search for genes expressed in different tissues, or download the dataset in a tabular form.
Conclusions
These data provide the basis for a gene expression atlas, which will facilitate functional genomic studies in common bean. Analysis of this dataset has identified genes important in regulating seed composition and has increased our understanding of nodulation and impact of the nitrogen source on assimilation and distribution throughout the plant.
【 授权许可】
2014 O’Rourke et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J: Beans (Phaseolus spp.) - model food legumes. Plant Soil 2003, 252:55-128.
- [2]Graham PH, Vance CP: Legumes: importance and constraints to greater use. Plant Physiol 2003, 131:872-877.
- [3]Ramirez M, Graham MA, Blanco-Lopez L, Silvente S, Medrano-Soto A, Blair MW, Hernandez G, Vance CP, Lara M: Sequencing and analysis of common bean ESTs, building a foundation for functional genomics. Plant Physiol 2005, 137:1211-1227.
- [4]Tian J, Venkatachalam P, Liao H, Yan X, Raghothama K: Molecular cloning and characterization of phosphorus starvation responsive genes in common bean (Phaseolus vulgaris L.). Planta 2007, 227:151-165.
- [5]Hernandez G, Ramirez M, Valdes-Lopez O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F, Wu HC, Lara M, Town CD, Kopka J, Udvardi MK, Vance CP: Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 2007, 144:752-767.
- [6]Thibivilliers S, Joshi T, Campbell KB, Scheffler B, Xu D, Coopers B, Nguyen HT, Stacey G: Generation of Phaseolus vulgaris ESTs and investigation of their regulation upon Uromyces appendiculatus infection. BMC Plant Biol 2009, 9:46. BioMed Central Full Text
- [7]Melotto M, Monteiro-Vitorello CB, Bruschi AG, Carmargo LE: Comparative bioinformatic analysis of genes expressed in common bean (Phaseolus vulgaris L.) seedlings. Genome 2005, 48:562-570.
- [8]Kalavacharia V, Liu Z, Meyers BC, Thimmapuram J, Melmaiee K: Identification and analysis of common bean (Phaseolus vulgaris L.) transcriptomes by massively parallel pyrosequencing. BMC Plant Biol 2011, 11:135. 107 BioMed Central Full Text
- [9]Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J, Jenkins J, Shu S, Song Q, Chavarro C: A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 2014, 46(7):707-713.
- [10]Lin J-Y, Stupar RM, Hans C, Hyten DL, Jackson SA: Structural and functional divergence of a 1-Mb duplicated region in the soybean (Glycine max) genome and comparison to an orthologous region from Phaseolus vulgaris. Plant Cell 2010, 22:2545-2561.
- [11]McClean PE, Marnidi S, McConnell M, Chikara S, Lee R: Synteny mapping between common bean and soybean reveals extensive blocks of shared loci. BMC Genomics 2010, 11:184-194. BioMed Central Full Text
- [12]Schlueter JA, Dixon P, Granger C, Grant D, Clark L, Doyle JJ, Shoemaker RC: Mining EST databases to resolve evolutionary events in major crop species. Genome 2004, 47:868-876.
- [13]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, 14:178-183.
- [14]Li J, Dai X, Liu T, Zhao PX: LegumeIP: an integrative database for comparative genomics and transcriptomics of model legumes. Nucleic Acids Res 2011, 40(D1):D1221-D1229.
- [15]Smith PMC, Atkins CA: Purine biosynthesis. Big in cell division, even bigger in nitrogen assimilation. Plant Physiol 2002, 128:793-802.
- [16]Ishisuka J: Function of Symbiotically Fixed Nitrogen for Grain Production in Soybean. In Proceedings of the International Seminar on Soil Intensive Agriculture. Tokyo, Japan: Society of the Science of Soil and Manure; 1977:617-624.
- [17]Thomas RJ, Schrader LE: The assimilation of ureides in shoot tissues of soybeans: changes in allantoinase activity and ureide contents of leaves and fruits. Plant Physiol 1981, 67:973-976.
- [18]Pelissier HC, Frerich A, Desimone M, Schumacher K, Tegeder M: PvUPS1, an allantoin transporter in nodulated roots of French bean. Plant Physiol 2004, 134(2):664-675.
- [19]Chen J, Huang B, Li Y, Du H, Gu Y, Liu H, Zhang J, Huang Y: Synergistic influence of sucrose and abscisic acid on the genes involved in starch synthesis in maize endosperm. Carbohydr Res 2011, 346:1684-1691.
- [20]Wang Z, Libault M, Joshi T, Valliyodan B, Nguyen HT, Xu D, Stacey G, Cheng J: SoyDB: a knowledge database of soybean transcription factors. BMC Plant Biol 2010, 10:14. BioMed Central Full Text
- [21]Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Hovath S, Drews GN, Fischer RL, Okamuro JK, Harada JJ, Goldberg RB: Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci U S A 2010, 107:8063-8070.
- [22]Verdier J, Kaker K, Gallardo K, Le Signor C, Aubert G, Schlereth A, Town CD, Udvardi MK, Thompson RD: Gene expression profileing of M. truncatula transcription factors identifies putative regulators of grain legume seed filling. Plant Mol Biol 2008, 67:567-580.
- [23]Le BH, Wagmaister JA, Bui AQ, Harada JJ, Goldberg RB: Using genomics to study legume seed development. Plant Physiol 2007, 144:562-574.
- [24]Hajduch M, Ganapathy A, Stein JW, Thelen JJ: A systematic proteomic study of seed filling in soybean. Establishment of high-resolution two-dimensional reference maps, expression profiles, and an interactive proteome database. Plant Physiol 2005, 137:1397-1419.
- [25]Bolon Y-T, Vance CP: Characterization of the Linkage Group I Seed Protein QTL in Soybean. In Designing Soybeans for the 21st Century. Edited by Wilson RF. Urbana: AOCS Press; 2012:175-195.
- [26]Severin AJ, Woody JL, Bolon Y-T, Joseph B, Diers BW, Farmer AD, Muehlbauer GJ, Nelson RT, Grant D, Specht JE, Graham MA, Cannon SB, May GD, Vance CP, Shoemaker RC: RNA-Seq atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol 2010, 10:160. BioMed Central Full Text
- [27]Weber H, Borisjuk L, Wobus U: Molecular physiology of legume seed development. Annu Rev Plant Biol 2005, 56:253-279.
- [28]Angeles-Nunez JG, Tiessen A: Arabidopsis sucrose synthase 2 and 3 modulate metabolic homeostasis and direct carbon towards starch synthesis in developing seeds. Planta 2010, 232(3):701-718.
- [29]Okuley J, Lightner J, Feldmann K, Yadav N, Lark E, Browse J: Arabidopsis FAD2 gene encodes the enzyme that is essential for polyunsaturated lipid synthesis. Plant Cell 1994, 6(1):147-158.
- [30]Verdier J, Thompson RD: Transcriptional regulation of storage protein synthesis during dicotyledon seed filling. Plant Cell Physiol 2008, 49(9):1263-1271.
- [31]Angeles-Nunez JG, Tiessen A: Mutation of the transcription factor LEAFY COTYLEDON 2 alters the chemical composition of Arabidopsis seeds, decreasing oil and protein content, while maintaining high levels of starch and sucrose in mature seeds. J Plant Physiol 2011, 168:1891-1900.
- [32]Gutierrez L, Van Wuytswinkel O, Catelain M, Bellini C: Combined networks regulating seed maturation. Trends Plant Sci 2007, 12:294-300.
- [33]Kanno Y, Jikumaru Y, Hanada A, Nambara E, Abrams SR, Kamiya Y, Seo M: Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant Cell Physiol 2010, 51(12):1988-2001.
- [34]Lefebvre V, North N, Frey A, Sotta B, Seo M, Okamoto M, Nambara E, Marion-Poll A: Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesize in the endosperm is involved in the induction of seed dormancy. Plant J 2006, 45:309-319.
- [35]Frey A, Effroy D, Lefebvre V, Seo M, Perreau F, Berger A, Sechet J, To A, North HM, Marion-Poll A: Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. The. Plant J 2012, 70(3):501-512.
- [36]Eastmond PJ, van Dijken AJ, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JD, Smeekens SC, Graham IA: Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis is essential for Arabidopsis embryo maturation. Plant J 2002, 29:225-235.
- [37]Barraza A, Estrada-Navarrete G, Rodriguez-Alegria ME, Lopez-Munguia A, Merino E, Quinto C, Sanchez F: Down-regulation of PvTRE1 enhances nodule biomass and bacteroid number in the common bean. New Phytol 2013, 197:194-206.
- [38]Gomez LD, Gilday A, Feil R, Lunn JE, Graham IA: AtTPS1-mediated trehalose 6-phosphate synthesis is essential for embryogenic and vegetative growth and responsiveness to ABA in germinating seeds and stomatal guard cells. Plant J 2010, 64:1-13.
- [39]Finke RL, Harper JE, Hageman RH: Efficiency of nitrogen assimilation by N2-fixing and nitrate grown soybean plants (Glycine max [L.] Merr.). Plant Physiol 1982, 70:1178-1184.
- [40]Timpo EE, Neyra CA: Expression of nitrate and nitrite reductase activities under various forms of nitrogen nutrition in Phaseolus vulgaris L. Plant Physiol 1983, 72:71-75.
- [41]Libault M, Farmer A, Joshi T, Takahashi K, Langley RJ, Franklin LD, He J, Xu D, May G, Stacey G: An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J 2010, 63:86-99.
- [42]Kouchi H, Imaizumi-Anraku H, Hayashi M, Hakoyama T, Nakagawa T, Umehara Y, Suganuma N, Kawaguchi M: How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol 2010, 51(9):1381-1397.
- [43]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.
- [44]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(6):680-689.
- [45]Oka-Kira E, Kawaguchi M: Long-distance signaling to control root nodule number. Curr Opin Plant Biol 2006, 9(5):496-502.
- [46]Reid DE, Ferguson BJ, Gresshoff PM: Inoculation and nitrate induced CLE peptides of soybean control NARK-dependent nodule formation. Mol Plant Microbe Interact 2011, 24:606-618.
- [47]Rival P, de Billy F, Bono JJ, Gouch C, Rosenberg C, Bensmihen S: Epidermal and cortical roles of NFP and DMI3 in coordinating early steps of nodulation in Medicago truncatula. Development 2012, 139:3383-3391.
- [48]Desbrosses GJ, Stougaard J: Root Nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host & Microbe 2011, 10:348-358.
- [49]Hayashi T, Shimoda Y, Sato S, Tabata S, Imaizumi-Anraku H, Hayashi M: Rhizobial infection does not require cortical expression of upstream common symbiosis genes responsible for the induction of Ca2+ spiking. Plant J 2014, 77:146-159.
- [50]Haney CH, Riely BK, Tricoli DM, Cook DR, Ehrhardt DW, Long SR: Symbiotic rhizobia bacteria trigger a change in localization and dynamics of the Medicago truncatula receptor kinase LYK3. Plant Cell 2011, 23:2774-2787.
- [51]Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, Barker DG, de Carvlho-Niebel F: AP2-ERF transcription factors mediate nod factor dependent Mt ENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 2007, 19:2866-2885.
- [52]Cerri MR, Frances L, Laloum T, Auriac MC, Niebel A, Oldroyd GE, Barker DG, Fournier J, de Carvlho-Niebel F: Medicago truncatula ERN transcription factors: regulatory interplay with NSP1/NSP2 expression dynamics throughout rhizobial infection. Plant Physiol 2012, 160:2155-2172.
- [53]Murray JD, Muni RR, Torres-Jerez I, Tang Y, Allen S, Andriankaja M, Li G, Laxmi A, Cheng X, Wen J, Vaughan D, Schultze M, Sun J, Charpentier M, Oldroyd G, Tadege M, Ratet P, Mysore KS, Chen R, Udvardi MK: Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula. Plant J 2011, 65:244-252.
- [54]Mergaert P, Nikovicks K, Kelemen Z, Maunoury N, Vaubert D, Kondorosi A, Kondorosi E: A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol 2003, 132:161-173.
- [55]Arrighi J-F, Godfroy O, de Billy F, Saurat O, Jauneau A, Gough C: The RPG gene of Medicago truncatula controls Rhizobium-directed polar growth during infection. Proc Natl Acad Sci U S A 2008, 105(28):9817-9822.
- [56]Oldroyd GED, Downie JA: Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Physiol Plant Mol Biol 2008, 59:519-546.
- [57]Haney CH, Long SR: Plant flotillins are required for infection by nitrogen-fixing bacteria. Proc Natl Acad Sci U S A 2010, 107:478-483.
- [58]Mbengue M, Camut S, de Carvlho-Niebel F, Deslandes L, Froidure S, Klaus-Heisen D, Moreau S, Rivas S, Timmers T, Herve C, Cullimore J, Lefebyre B: The Medicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell 2010, 22:3474-3488.
- [59]Fang Y, Hirsch AM: Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in transgenic alfalfa. Plant Physiol 1998, 116:53-68.
- [60]Combier J-P, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernie 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.
- [61]Chen L-Q, Qu X-Q, Hou B-H, Sosso D, Osorio S, Fernie AR, Frommer WB: Sucrose efflux mediated by SWEET proteins ad a key step for phloem transport. Science 2012, 335:207-211.
- [62]Chen L-Q, Hou B-H, Lalonde S, Takanaga H, Hartung ML, Qu X-Q, Guo W-J, Kim J-G, Underwood W, Chaudhuri B, Chermak D, Antony G, White FF, Somerville SC, Mudgett MB, Frommer WB: Sugar transporters for intercellular exhange and nutrition of pathogens. Nature 2010, 468:527-532.
- [63]de Carvalho GA B, Stefania J, Batista S, Marcelino-Guimaraes FC, Costa do Nascimento L, Hungria M: Transcriptional analysis of genes involved in nodulation in soybean roots inoculated with Bradyrhizobium japonicum strain CPAC 15. BMC Genomics 2013, 14:153. BioMed Central Full Text
- [64]Schauser L, Roussis A, Stiller J, Stougaard J: A plant regulator controlling development of symbiotic root nodules. Nature 1999, 402:191-195.
- [65]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:e:1003352.
- [66]Konishi M, Yanagisawa S: Arabidopsis NIN-like transcription factors have a central role in nitrate signaling. Nat Commun 2013, 4:1617.
- [67]Capoen W, Oldroyd G: How CYCLOPS keeps an eye on plant symbiosis. Proc Natl Acad Sci U S A 2008, 105:20053-20054.
- [68]Madsen LH, Trichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, Ronson CW, James EK, Stougaard J: The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 2010., 1doi:10.1038/ncomms1009
- [69]Yano K, Shibata S, Chen WL, Sato S, Kaneko T, Jurkiewicz A, Sandal N, Banba M, Imaizumi-Anraku H, Kojima T, Ohtomo R, Szczyglowski K, Stougaard J, Tabata S, Hayashi M, Kouchi H, Umehara Y: CERBERUS, a novel U-box protein containing WD-40 repeats, is required for formation of the infection thread and nodule development in the legume-rhizobium symbiosis. Plant J 2009, 60:168-180.
- [70]Krusell L, Krause K, Ott T, Desbrosses G, Kramer U, Sato S, Nakamura Y, Tabata S, James EK, Sandal N, Stougaard J, Kawaguchi M, Miyamoto A, Suganuma N, Udvardi MK: The sulfate transporter SST1 is crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules. Plant Cell 2005, 17:1625-1636.
- [71]Ott T, van Dongen JT, Gunther C, Krusell L, Desbrosses G, Vigeolas H, Bock V, Czechowski T, Geigenberger P, Udvardi MK: Symbiotic leghemoglobins are crucial for nitrogen fixing in legume root nodules but not for general plant growth and development. Curr Biol 2005, 15:531-535.
- [72]Blanco L, Reddy PM, Silvente S, Bucciarelli B, Khandual S, Alvarado-Affantranger X, Sanchez F, Miller S, Vance C, Lara-Flores M: Molecular cloning, characterization and regulation of two different NADH-glutamate synthase cDNAs in bean nodules. Plant Cell Environ 2008, 3:454-472.
- [73]Olivares JE, Diaz-Camino C, Estrada-Navarrete G, Alvarado-Affantranger X, Rodriguez-Kessler M, Samudio FZ, Olamendi-Portugal T, Marquez Y, Servin LE, Sanchez F: Nodulin 41, a novel late nodulin of common bean with peptidase activity. BMC Plant Biol 2011, 11:134. BioMed Central Full Text
- [74]Charpentier M, Bredemeier R, Wanner G, Takeda N, Schleiff E, Parniske M: Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 2008, 20:3467-3479.
- [75]DeYoung BJ, Innes RW: Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 2006, 7(12):1243-1249.
- [76]Heyl A, Schmuling T: Cytokinin signal perception and transduction. Curr Opin Plant Biol 2003, 6:480-488.
- [77]Lohar DP, Schaff JE, Laskey JG, Kieber JJ, Bilyeu KD, Bird DM: Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. Plant J 2004, 38:203-214.
- [78]Pottosin I, Velarde-Buendia AM, Bose J, Zepeda-Jazo I, Shabala S, Dobrovinskaya O: Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. J Exp Bot 2014. doi:10.1093/jxb/ert1423
- [79]Zepeda-Jazo I, Velarde-Buendia AM, Enriquez-Figueroa R, Bose J, Shabala S, Muniz-Murguia J, Pottosin II: Polyamines interact with hydroxy radicals in activating Ca2+ and K+ transport across the root epidermal plasma membranes. Plant Physiol 2011, 157:2167-2180.
- [80]Kiba T, Kudo T, Kojima M, Sakakibara H: Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 2011, 62:1399-1409.
- [81]Okamoto M, Kumar A, Li W, Wang Y, Yaeesh-Siddiqi M, Crawford NM, Glass ADM: High-affinity nitrate transport in roots of Arabidopsis depends on expression of the NAR2-like gene AtNRT3.1. Plant Physiol 2006, 140:1036-1046.
- [82]Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM: Nitrate transport and signaling. J Exp Bot 2007, 58:2297-2306.
- [83]Tsay YF, Chiu CC, Tsai CB, Ho CH, Hsu PK: Nitrate transporters and peptide transporters. FEBS Lett 2007, 581:2290-2300.
- [84]Gojon A, Nacry P, Davidian JC: Root uptake regulation: a central process for NPS homeostasis in plants. Curr Opin Plant Biol 2009, 12:328-338.
- [85]Bouguyon E, Gojon A, Nacry P: Nitrate sensing and signaling in plants. Semin Cell Dev Biol 2012, 23:648-654.
- [86]Gojon A, Krouk G, Perrine-Walker F, Laugier E: Nitrate transceptor(s) in plants. J Exp Bot 2011, 62:2299-2308.
- [87]Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K, Zazimalova E, Benkova E, Nacry P, Gojon A: Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 2010, 18:927-937.
- [88]Miflin BJ, Habash DZ: The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J Exp Bot 2002, 53:979-987.
- [89]McGrath RB, Coruzzi GM: A gene network controlling glutamine and asparagine biosynthesis in plants. Plant J 1991, 3:275-280.
- [90]O’Rourke JA, Yang SS, Miller SS, Bucciarelli B, Liu J, Rydeen A, Bozsoki Z, Uhde-Stone C, Tu ZJ, Allan D, Gronwald JW, Vance CP: An RNA-Seq transcriptome analysis of orthophosphate-deficient white lupin reveals novel insights into phosphorus acclimation in plants. Plant Physiol 2013, 161:705-724.
- [91]Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. BioMed Central Full Text
- [92]Mortazavi A, Williams BA, McCue K, Schaffer L, Wold B: Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5(7):621-628.
- [93]Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M: The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 2008, 320(5881):1344-1349.
- [94]Zhao J, Oshumi TK, Kung JT, Ogawa Y, Grau DJ, Sarma K, Song JJ, Kingston RE, Borowsky M, Lee JT: Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell 2010, 40:939-953.
- [95]Burke GR, Strand MR: Deep sequencing identifies viral and wasp genes with potential roles in replication of Microplitis demolitor bracovirus. J Virol 2012, 86:3293-3306.
- [96]Tarazona S, Garcia-Alcalde F, Dopazo J, Ferrer A, Conesa A: Differential expression in RNA-seq: a matter of depth. Genome Res 2011, 21:2213-2223.
- [97]Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible W-R: Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 2005, 139(1):5-17.
- [98]Borges A, Tsai SM, Caldes DGG: Validation of reference genes for RT-qPCR normalization in common bean during biotic and abiotic stresses. Plant Cell Rep 2012, 31:827-838.
- [99]Vance CP, Heichel GH, Barnes DK, Bryan JW, Johnson LE: Nitrogen fixation, nodule development, and vegetative regrowth of alfalfa (Medicago sativa L.) following harvest. Plant Physiol 1979, 64:1-8.
- [100]Sbabou L, Bucciarelli B, Miller SS, Liu J, Berhada F, Filali-Maltouf A, Allan D, Vance CP: Molecular analysis of SCARECROW genes expressed in white lupin cluster roots. J Exp Bot 2010, 61(5):1351-1363.