BMC Genomics | |
RNA-seq analysis identifies an intricate regulatory network controlling cluster root development in white lupin | |
Oliver Berkowitz1  James Whelan3  Huixia Shou2  David Secco4  | |
[1] School of Plant Biology, University of Western Australia, Crawley, WA 6009, Australia;Joint Research Laboratory in Genomics and Nutriomics, College of Life Sciences, Zhejiang University, Hangzhou 310058, China;Department of Botany, School of Life Science, La Trobe University, Bundoora, Victoria 3086, Australia;Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, WA 6009, Australia | |
关键词: de novo transcriptome; RNA-seq; Phosphate; Root development; White lupin; Cluster root; | |
Others : 1217645 DOI : 10.1186/1471-2164-15-230 |
|
received in 2014-01-14, accepted in 2014-03-18, 发布年份 2014 | |
【 摘 要 】
Background
Highly adapted plant species are able to alter their root architecture to improve nutrient uptake and thrive in environments with limited nutrient supply. Cluster roots (CRs) are specialised structures of dense lateral roots formed by several plant species for the effective mining of nutrient rich soil patches through a combination of increased surface area and exudation of carboxylates. White lupin is becoming a model-species allowing for the discovery of gene networks involved in CR development. A greater understanding of the underlying molecular mechanisms driving these developmental processes is important for the generation of smarter plants for a world with diminishing resources to improve food security.
Results
RNA-seq analyses for three developmental stages of the CR formed under phosphorus-limited conditions and two of non-cluster roots have been performed for white lupin. In total 133,045,174 high-quality paired-end reads were used for a de novo assembly of the root transcriptome and merged with LAGI01 (Lupinus albus gene index) to generate an improved LAGI02 with 65,097 functionally annotated contigs. This was followed by comparative gene expression analysis. We show marked differences in the transcriptional response across the various cluster root stages to adjust to phosphate limitation by increasing uptake capacity and adjusting metabolic pathways. Several transcription factors such as PLT, SCR, PHB, PHV or AUX/IAA with a known role in the control of meristem activity and developmental processes show an increased expression in the tip of the CR. Genes involved in hormonal responses (PIN, LAX, YUC) and cell cycle control (CYCA/B, CDK) are also differentially expressed. In addition, we identify primary transcripts of miRNAs with established function in the root meristem.
Conclusions
Our gene expression analysis shows an intricate network of transcription factors and plant hormones controlling CR initiation and formation. In addition, functional differences between the different CR developmental stages in the acclimation to phosphorus starvation have been identified.
【 授权许可】
2014 Secco et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150707171944451.pdf | 3119KB | download | |
Figure 7. | 53KB | Image | download |
Figure 6. | 138KB | Image | download |
Figure 5. | 123KB | Image | download |
Figure 4. | 108KB | Image | download |
Figure 3. | 203KB | Image | download |
Figure 2. | 137KB | Image | download |
Figure 1. | 77KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.
【 参考文献 】
- [1]Gerke J: Phosphate, aluminum and iron in the soil solution of 3 different soils in relation to varying concentrations of citric acid. Z Pflanz Bodenkunde 1992, 155:339-343.
- [2]Scholz RW, Wellmer FW: Approaching a dynamic view on the availability of mineral resources: what we may learn from the case of phosphorus? Global Environ Change-Human and Policy Dimensions 2013, 23:11-27.
- [3]Chiou TJ, Lin SI: Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 2011, 62:185-206.
- [4]Essigmann B, Guler S, Narang RA, Linke D, Benning C: Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A 1998, 95:1950-1955.
- [5]Secco D, Wang C, Arpat BA, Wang Z, Poirier Y, Tyerman SD, Wu P, Shou H, Whelan J: The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytol 2012, 193:842-851.
- [6]Bari R, Datt Pant B, Stitt M, Scheible WR: PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 2006, 141:988-999.
- [7]Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ: pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 2006, 141:1000-1011.
- [8]Liu TY, Huang TK, Tseng CY, Lai YS, Lin SI, Lin WY, Chen JW, Chiou TJ: PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell 2012, 24:2168-2183.
- [9]Huang TK, Han CL, Lin SI, Chen YJ, Tsai YC, Chen YR, Chen JW, Lin WY, Chen PM, Liu TY, Chen YS, Sun CM, Chiou TJ: Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in arabidopsis roots. Plant Cell 2013, 25:4044-4066.
- [10]Peret B, Clement M, Nussaume L, Desnos T: Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 2011, 16:442-450.
- [11]Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ: Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 2006, 98:693-713.
- [12]Neumann G, Martinoia E: Cluster roots–an underground adaptation for survival in extreme environments. Trends Plant Sci 2002, 7:162-167.
- [13]Cheng L, Bucciarelli B, Shen J, Allan D, Vance CP: Update on lupin cluster roots: update on white lupin cluster root acclimation to phosphorus deficiency. Plant Physiol 2011, 156:1025-1032.
- [14]Shane MW, De Vos M, De Roock S, Lambers H: Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system. Plant Cell Environ 2003, 26:265-273.
- [15]Shu LZ, Shen JB, Rengel Z, Tang CX, Zhang FS: Cluster root formation by Lupinus albus is modified by stratified application of phosphorus in a split-root system. J Plant Nutr 2007, 30:271-288.
- [16]Watt M, Evans JR: Linking development and determinacy with organic acid efflux from proteoid roots of white lupin grown with low phosphorus and ambient or elevated atmospheric CO2 concentration. Plant Physiol 1999, 120:705-716.
- [17]Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L: Lateral root development in arabidopsis: fifty shades of auxin. Trends Plant Sci 2013, 18:450-458.
- [18]Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L: Phosphate availability alters architecture and causes changes in hormone sensitivity in the arabidopsis root system. Plant Physiol 2002, 129:244-256.
- [19]Perez-Torres CA, Lopez-Bucio J, Cruz-Ramirez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L: Phosphate availability alters lateral root development in arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 2008, 20:3258-3272.
- [20]Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P: A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in arabidopsis. Plant Physiol 2005, 138:2061-2074.
- [21]Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB, Offringa R, Graham N, Doumas P, Friml J, Bogusz D, Beeckman T, Bennett M: Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 2007, 19:3889-3900.
- [22]Bielach A, Podlesakova K, Marhavy P, Duclercq J, Cuesta C, Muller B, Grunewald W, Tarkowski P, Benkova E: Spatiotemporal regulation of lateral root organogenesis in arabidopsis by cytokinin. Plant Cell 2012, 24:3967-3981.
- [23]Dello Ioio R, Galinha C, Fletcher AG, Grigg SP, Molnar A, Willemsen V, Scheres B, Sabatini S, Baulcombe D, Maini PK, Tsiantis M: A PHABULOSA/cytokinin feedback loop controls root growth in arabidopsis. Curr Biol 2012, 22:1699-1704.
- [24]Gilbert GA, Knight JD, Vance CP, Allan DL: Proteoid root development of phosphorus deficient lupin is mimicked by auxin and phosphonate. Ann Bot 2000, 85:921-928.
- [25]Meng ZB, You XD, Suo D, Chen YL, Tang C, Yang JL, Zheng SJ: Root-derived auxin contributes to the phosphorus-deficiency-induced cluster-root formation in white lupin (Lupinus albus). Physiol Plant 2013, 148:481-489.
- [26]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.
- [27]Neumann G, Massonneau A, Langlade N, Dinkelaker B, Hengeler C, Romheld V, Martinoia E: Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Ann Bot 2000, 85:909-919.
- [28]Schulz MH, Zerbino DR, Vingron M, Birney E: Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 2012, 28:1086-1092.
- [29]Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M: mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 2004, 37:914-939.
- [30]Juszczuk I, Malusà E, Rychter AM: Oxidative stress during phosphate deficiency in roots of bean plants (Phaseolus vulgaris L.). J Plant Physiol 2001, 158:1299-1305.
- [31]Torabi S, Wissuwa M, Heidari M, Naghavi MR, Gilany K, Hajirezaei MR, Omidi M, Yazdi-Samadi B, Ismail AM, Salekdeh GH: A comparative proteome approach to decipher the mechanism of rice adaptation to phosphorous deficiency. Proteomics 2009, 9:159-170.
- [32]Tsukagoshi H, Busch W, Benfey PN: Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 2010, 143:606-616.
- [33]Chang L, Ramireddy E, Schmulling T: Lateral root formation and growth of Arabidopsis is redundantly regulated by cytokinin metabolism and signalling genes. J Exp Bot 2013, 64:5021-5033.
- [34]Franco-Zorrilla JM, Martin AC, Leyva A, Paz-Ares J: Interaction between phosphate-starvation, sugar, and cytokinin signaling in arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol 2005, 138:847-857.
- [35]Zhu YY, Zeng HQ, Dong CX, Yin XM, Shen QR, Yang ZM: microRNA expression profiles associated with phosphorus deficiency in white lupin (Lupinus albus L.). Plant Sci 2010, 178:23-29.
- [36]Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ: Uncovering small RNA-mediated responses to phosphate-deficiency in arabidopsis by deep sequencing. Plant Physiol 2009, 151:2120-2132.
- [37]Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrerra-Estrella L, Nussaume L, Thibaud MC: A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci U S A 2005, 102:11934-11939.
- [38]Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, Blasing O, Usadel B, Czechowski T, Udvardi MK, Stitt M, Scheible WR: Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell and Environ 2007, 30:85-112.
- [39]Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, Deng XW: Phosphate starvation triggers distinct alterations of genome expression in arabidopsis roots and leaves. Plant Physiol 2003, 132:1260-1271.
- [40]Zheng L, Huang F, Narsai R, Wu J, Giraud E, He F, Cheng L, Wang F, Wu P, Whelan J, Shou H: Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol 2009, 151:262-274.
- [41]Wang S, Zhang S, Sun C, Xu Y, Chen Y, Yu C, Qian Q, Jiang DA, Qi Y: Auxin response factor (OsARF12), a novel regulator for phosphate homeostasis in rice (Oryza sativa). New Phytol 2014, 201:91-103.
- [42]Secco D, Jabnoune M, Walker H, Shou H, Wu P, Poirier Y, Whelan J: Spatio-temporal transcript profiling of rice roots and shoots in response to phosphate starvation and recovery. Plant Cell 2013, 25:4285-4304.
- [43]Massonneau A, Langlade N, Leon S, Smutny J, Vogt E, Neumann G, Martinoia E: Metabolic changes associated with cluster root development in white lupin (Lupinus albus L.): relationship between organic acid excretion, sucrose metabolism and energy status. Planta 2001, 213:534-542.
- [44]Linkohr BI, Williamson LC, Fitter AH, Leyser HM: Nitrate and phosphate availability and distribution have different effects on root system architecture of arabidopsis. Plant J 2002, 29:751-760.
- [45]Rouached H, Secco D, Arpat B, Poirier Y: The transcription factor PHR1 plays a key role in the regulation of sulfate shoot-to-root flux upon phosphate starvation in Arabidopsis. BMC Plant Biol 2011, 11:19. BioMed Central Full Text
- [46]Kant S, Peng M, Rothstein SJ: Genetic regulation by NLA and MicroRNA827 for maintaining nitrate-dependent phosphate homeostasis in arabidopsis. PLoS Genet 2011, 7:e1002021.
- [47]Ticconi CA, Lucero RD, Sakhonwasee S, Adamson AW, Creff A, Nussaume L, Desnos T, Abel S: ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc Natl Acad Sci U S A 2009, 106:14174-14179.
- [48]Bournier M, Tissot N, Mari S, Boucherez J, Lacombe E, Briat J-F, Gaymard F: Arabidopsis ferritin 1 (AtFer1) gene regulation by the phosphate starvation response 1 (AtPHR1) transcription factor reveals a direct molecular link between iron and phosphate homeostasis. J Biol Chem 2013, 288:22670-22680.
- [49]Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG: The effect of iron on the primary root elongation of arabidopsis during phosphate deficiency. Plant Physiol 2008, 147:1181-1191.
- [50]Coudert Y, Perin C, Courtois B, Khong NG, Gantet P: Genetic control of root development in rice, the model cereal. Trends Plant Sci 2010, 15:219-226.
- [51]Petricka JJ, Winter CM, Benfey PN: Control of arabidopsis root development. Annu Rev Plant Biol 2012, 63:563-590.
- [52]Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B: The PIN auxin efflux facilitator network controls growth and patterning in arabidopsis roots. Nature 2005, 433:39-44.
- [53]Grieneisen VA, Xu J, Maree AF, Hogeweg P, Scheres B: Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 2007, 449:1008-1013.
- [54]Swarup K, Benkova E, Swarup R, Casimiro I, Peret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K, Jones JD, Taylor CG, Schachtman DP, May S, Sandberg G, Benfey P, Friml J, Kerr I, Beeckman T, Laplaze L, et al.: The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 2008, 10:946-954.
- [55]Vanneste S, Friml J: Auxin: a trigger for change in plant development. Cell 2009, 136:1005-1016.
- [56]Zhou W, Wei L, Xu J, Zhai Q, Jiang H, Chen R, Chen Q, Sun J, Chu J, Zhu L, Liu CM, Li C: Arabidopsis Tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 2010, 22:3692-3709.
- [57]Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, McSteen P, Zhao Y, Hayashi K, Kamiya Y, Kasahara H: The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci U S A 2011, 108:18512-18517.
- [58]Qin G, Gu H, Zhao Y, Ma Z, Shi G, Yang Y, Pichersky E, Chen H, Liu M, Chen Z, Qu LJ: An indole-3-acetic acid carboxyl methyltransferase regulates arabidopsis leaf development. Plant Cell 2005, 17:2693-2704.
- [59]Ranocha P, Denance N, Vanholme R, Freydier A, Martinez Y, Hoffmann L, Kohler L, Pouzet C, Renou JP, Sundberg B, Boerjan W, Goffner D: Walls are thin 1 (WAT1), an Arabidopsis homolog of Medicago truncatula NODULIN21, is a tonoplast-localized protein required for secondary wall formation in fibers. Plant J 2010, 63:469-483.
- [60]Wan YL, Jasik J, Wang L, Hao HQ, Volkmann D, Menzel D, Mancuso S, Baluska F, Lin JX: The signal transducer NPH3 integrates the Phototropin1 photosensor with PIN2-based polar auxin transport in arabidopsis root phototropism. Plant Cell 2012, 24:551-565.
- [61]Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B: PLETHORA proteins as dose-dependent master regulators of arabidopsis root development. Nature 2007, 449:1053-1057.
- [62]Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vaten A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN: Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 2010, 465:316-321.
- [63]Jang G, Yi K, Pires ND, Menand B, Dolan L: RSL genes are sufficient for rhizoid system development in early diverging land plants. Development 2011, 138:2273-2281.
- [64]Karas B, Amyot L, Johansen C, Sato S, Tabata S, Kawaguchi M, Szczyglowski K: Conservation of lotus and arabidopsis basic helix-loop-helix proteins reveals new players in root hair development. Plant Physiol 2009, 151:1175-1185.
- [65]Menand B, Yi K, Jouannic S, Hoffmann L, Ryan E, Linstead P, Schaefer DG, Dolan L: An ancient mechanism controls the development of cells with a rooting function in land plants. Science 2007, 316:1477-1480.
- [66]Wang P, Du Y, Zhao X, Miao Y, Song CP: The MPK6-ERF6-ROS-responsive cis-acting element7/GCC box complex modulates oxidative gene transcription and the oxidative response in arabidopsis. Plant Physiol 2013, 161:1392-1408.
- [67]Shin R, Berg RH, Schachtman DP: Reactive oxygen species and root hairs in arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 2005, 46:1350-1357.
- [68]Khan GA, Declerck M, Sorin C, Hartmann C, Crespi M, Lelandais-Briere C: MicroRNAs as regulators of root development and architecture. Plant Mol Biol 2011, 77:47-58.
- [69]Pant BD, Buhtz A, Kehr J, Scheible WR: MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 2008, 53:731-738.
- [70]Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ: Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 2008, 147:732-746.
- [71]Laubinger S, Zeller G, Henz SR, Buechel S, Sachsenberg T, Wang J-W, Rätsch G, Weigel D: Global effects of the small RNA biogenesis machinery on the arabidopsis thaliana transcriptome. Proc Natl Acad Sci U S A 2010, 107:17466-17473.
- [72]Reyes JL, Chua N-H: ABA induction of miR159 controls transcript levels of two MYB factors during arabidopsis seed germination. Plant J 2007, 49:592-606.
- [73]Florez-Sarasa I, Lambers H, Wang X, Finnegan PM, Ribas-Carbo M: The alternative respiratory pathway mediates carboxylate synthesis in white lupin cluster roots under phosphorus deprivation. Plant, Cell Environ 2014, 37(4):922-928.
- [74]Li W, Godzik A: Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22:1658-1659.
- [75]Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676.
- [76]Kent WJ: BLAT–the BLAST-like alignment tool. Genome Res 2002, 12:656-664.
- [77]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
- [78]Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28:511-515.
- [79]Maere S, Heymans K, Kuiper M: BiNGO: a cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 2005, 21:3448-3449.
- [80]Gruber AR, Lorenz R, Bernhart SH, Neubock R, Hofacker IL: The vienna RNA websuite. Nucleic Acids Res 2008, 36:W70-74.