Global poplar root and leaf transcriptomes reveal links between growth and stress responses under nitrogen starvation and excess

Tree Physiology

Volumn 35, Issue 12, 2015, Pages 1283-1302

  Luo, Jie ^a,b   Zhou, Jing ^a   Li, Hong ^b   Shi, Wenguang ^a   Polle, Andrea ^c   Lu, Mengzhu ^a   Sun, Xiaomei ^a   Luo, Zhi Bin ^a,b  

^a RESEARCH INSTITUTE OF FORESTRY   (China)

^b NORTHWEST A F UNIVERSITY   (China)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

nutrient physiology; phytohormone; Populus; RNA sequencing; woody plants

Indexed keywords

ABSCISIC ACID; ACCLIMATION; AMINO ACID; DECIDUOUS TREE; GENE EXPRESSION; GENETIC ANALYSIS; GROWTH RESPONSE; HORMONE; LEAF; METABOLISM; MORPHOLOGY; NITROGEN; NUTRIENT AVAILABILITY; NUTRIENT UPTAKE; PHOTOSYNTHESIS; PHYSIOLOGICAL RESPONSE; RNA; ROOT SYSTEM; STARVATION; SURFACE AREA; WOODY PLANT;

POPULUS; POPULUS SIMONII;

AMMONIUM NITRATE; NITRIC ACID DERIVATIVE; PLANT PROTEIN; TRANSCRIPTOME;

DNA SEQUENCE; DOSE RESPONSE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; PLANT ROOT; POPULUS;

DOSE-RESPONSE RELATIONSHIP, DRUG; NITRATES; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; POPULUS; SEQUENCE ANALYSIS, DNA; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 84948828518     PISSN: 0829318X     EISSN: 17584469     Source Type: Journal    
DOI: 10.1093/treephys/tpv091     Document Type: Article

References (106)

1. Araya T, Miyamoto M, Wibowo J et al. (2014) CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proc Natl Acad Sci USA 111:2029-2034.
2. Bai H, Euring D, Volmer K, Janz D, Polle A (2013) The nitrate transporter (NRT) gene family in poplar. PLoS One 8:e72126. doi:10.1371/journal.pone.0072126
3. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202-W208.
4. Balasus A, Bischoff WA, Schwarz A, Scholz V, Kern J (2012) Nitrogen fluxes during the initial stage of willows and poplars in short-rotation coppices. J Plant Nutr Soil Sci 175:729-738.
5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289-300.
6. Bi YM, Meyer A, Downs GS, Shi X, El-Kereamy A, Lukens L, Rothstein SJ (2014) High throughput RNA sequencing of a hybrid maize and its parents shows different mechanisms responsive to nitrogen limitation. BMC Genomics 15:77.
7. Bilodeau-Gauthier S, Pare D, Messier C, Belanger N (2011) Juvenile growth of hybrid poplars on acidic boreal soil determined by environmental effects of soil preparation, vegetation control, and fertilization. For Ecol Manag 261:620-629.
8. Black BL, Fuchigami LH, Coleman GD (2002) Partitioning of nitrate assimilation among leaves, stems and roots of poplar. Tree Physiol 22:717-724.
9. Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14:1232-1238.
10. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
11. Brautigam A, Gagneul D, Weber AP (2007) High-throughput colorimetric method for the parallel assay of glyoxylic acid and ammonium in a single extract. Anal Biochem 362:151-153.
12. Brewitz E, Larsson CM, Larsson M (1995) Influence of nitrate supply on concentrations and translocation of abscisic acid in barley (Hordeum vulgare). Physiol Plant 95:499-506.
13. Brunner AM, Yakovlev IA, Strauss SH (2004) Validating internal controls for quantitative plant gene expression studies. BMC Plant Biol 4:14. doi:10.1186/1471-2229- 4-14
14. Canales J, Flores-Monterrosso A, Rueda-Lopez M, Avila C, Canovas FM (2010) Identification of genes regulated by ammonium availability in the roots of maritime pine trees. Amino Acids 39:991-1001.
15. Canales J, Moyano TC, Villarroel E, Gutierrez RA (2014) Systems analysis of transcriptome data provides new hypotheses about Arabidopsis root response to nitrate treatments. Front Plant Sci 5:22. doi:10.3389/fpls.2014.00022
16. Cao HH, Zhang M, Zhao H, Zhang Y, Wang XX, Guo SS, Zhang ZF, Liu TX (2014) Deciphering the mechanism of ß-aminobutyric acid-induced resistance in wheat to the grain aphid, Sitobion avenae. PLoS One 9:e91768. doi:10.1371/journal.pone.0091768
17. Cao X, Jia JB, Li H et al. (2012) Photosynthesis, water use efficiency and stable carbon isotope composition are associated with anatomical properties of leaf and xylem in six poplar species. Plant Biol 14:612-620.
18. Casazza AP, Rossini S, Rosso MG, Soave C (2005) Mutational and expression analysis of ELIP1 and ELIP2 in Arabidopsis thaliana. Plant Mol Biol 58:41-51.
19. Cooke JEK, Brown KA, Wu R, Davis JM (2003) Gene expression associated with N-induced shifts in resource allocation in poplar. Plant Cell Environ 26:757-770.
20. Cooke JEK, Martin TA, Davis JM (2005) Short-term physiological and developmental responses to nitrogen availability in hybrid poplar. New Phytol 167:41-52.
21. Coskun D, Britto DT, Li M, Becker A, Kronzucker HJ (2013) Rapid ammonia gas transport accounts for futile transmembrane cycling under NH3/NH4+ toxicity in plant roots. Plant Physiol 163:1859-1867.
22. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188-1190.
23. Delker C, Stenzel I, Hause B, Miersch O, Feussner I, Wasternack C (2006) Jasmonate biosynthesis in Arabidopsis thaliana-enzymes, products, regulation. Plant Biol 8:297-306.
24. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64-W70.
25. Ehlting B, Dluzniewska P, Dietrich H et al. (2007) Interaction of nitrogen nutrition and salinity in Grey poplar (Populus tremula × alba). Plant Cell Environ 30:796-811.
26. Euring D, Lofke C, Teichmann T, Polle A (2012) Nitrogen fertilization has differential effects on N allocation and lignin in two Populus species with contrasting ecology. Trees 26:1933-1942.
27. Euring D, Bai H, Janz D, Polle A (2014) Nitrogen-driven stem elongation in poplar is linked with wood modification and gene clusters for stress, photosynthesis and cell wall formation. BMC Plant Biol 14:391. doi:10.1186/s12870-014-0391-3
28. Fukaki H, Tasaka M (2009) Hormone interactions during lateral root formation. Plant Mol Biol 69:437-449.
29. Gojon A, Krouk G, Perrine-Walker F, Laugier E (2011) Nitrate transceptor(s) in plants. J Exp Bot 62:2299-2308.
30. Grant CE, Bailey TL, Noble WS (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics 27:1017-1018.
31. Gruffman L, Jamtgard S, Nasholm T (2014) Plant nitrogen status and co-occurrence of organic and inorganic nitrogen sources influence root uptake by Scots pine seedlings. Tree Physiol 34:205-213.
32. Gutierrez RA (2012) Systems biology for enhanced plant nitrogen nutrition. Science 336:1673-1675.
33. Hacke UG, Plavcova L, Almeida-Rodriguez A, King-Jones S, Zhou W, Cooke JEK (2010) Influence of nitrogen fertilization on xylem traits and aquaporin expression in stems of hybrid poplar. Tree Physiol 30:1016-1025.
34. Hamburger D, Rezzonico E, Petetot JMC, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14:889-902.
35. He J, Qin J, Long L et al. (2011) Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus × canescens. Physiol Plant 143:50-63.
36. He J, Li H, Luo J et al. (2013a) A transcriptomic network underlies microstructural and physiological responses to cadmium in Populus × canescens. Plant Physiol 162:424-439.
37. He J, Ma C, Ma Y, Li H, Kang J, Liu T, Polle A, Peng C, Luo ZB (2013b) Cadmium tolerance in six poplar species. Environ Sci Pollut Res 20:163-174.
38. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297-300.
39. Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62:1399-1409.
40. Krapp A, Berthome R, Orsel M et al. (2011) Arabidopsis roots and shoots show distinct temporal adaptation patterns toward nitrogen starvation. Plant Physiol 157:1255-1282.
41. Krouk G, Lacombe B, Bielach A et al. (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18:927-937.
42. Krouk G, Ruffel S, Gutierrez RA, Gojon A, Crawford NM, Coruzzil GM, Lacombe B (2011) A framework integrating plant growth with hormones and nutrients. Trends Plant Sci 16:178-182.
43. Kube M, Yang H, Richter GL et al. (2012) The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. Plant J 69:640-654.
44. Lam HM, Wong P, Chan HK, Yam KM, Chen L, Chow CM, Coruzzi GM (2003) Overexpression of the ASN1 gene enhances nitrogen status in seeds of Arabidopsis. Plant Physiol 132:926-935.
45. Li H, Li M, Luo J et al. (2012) N-fertilization has different effects on the growth, carbon and nitrogen physiology, and wood properties of slow- and fast-growing Populus species. J Exp Bot 63:6173-6185.
46. Li H, Li J, He Y, Li S, Liang Z, Peng C, Polle A, Luo Z-B (2013) Changes in carbon, nutrients and stoichiometric relations under different soil depths, plant tissues and ages in black locust plantations. Acta Physiol Plant 35:2951-2964.
47. Lin CC, Kao CH (1996) Disturbed ammonium assimilation is associated with growth inhibition of roots in rice seedlings caused by NaCl. Plant Growth Regul 18:233-238.
48. Loque D, Ludewig U, Yuan L, von Wiren N (2005) Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol 137:671-680.
49. Luo J, Li H, Liu T, Polle A, Peng C, Luo ZB (2013a) Nitrogen metabolism of two contrasting poplar species during acclimation to limiting nitrogen availability. J Exp Bot 64:4207-4224.
50. Luo J, Qin J, He F, Li H, Liu T, Polle A, Peng C, Luo ZB (2013b) Net fluxes of ammonium and nitrate in association with H+ fluxes in fine roots of Populus popularis. Planta 237:919-931.
51. Luo ZB, Polle A (2009) Wood composition and energy content in a poplar short rotation plantation on fertilized agricultural land in a future CO2 atmosphere. Glob Change Biol 15:38-47.
52. Luo Z-B, Calfapietra C, Scarascia-Mugnozza G, Liberloo M, Polle A (2008) Carbon-based secondary metabolites and internal nitrogen pools in Populus nigra under Free Air CO2 Enrichment (FACE) and nitrogen fertilisation. Plant Soil 304:45-57.
53. Luo ZB, Janz D, Jiang X, Gobel C, Wildhagen H, Tan Y, Rennenberg H, Feussner I, Polle A (2009a) Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol 151:1902-1917.
54. Luo ZB, Li K, Jiang X, Polle A (2009b) Ectomycorrhizal fungus (Paxillus involutus) and hydrogels affect performance of Populus euphratica exposed to drought stress. Ann For Sci 66:106.
55. Ma W, Li J, Qu B, He X, Zhao X, Li B, Fu X, Tong Y (2014a) Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis. Plant J 78:70-79.
56. Ma Y, He J, Ma C, Luo J, Li H, Liu T, Polle A, Peng C, Luo ZB (2014b) Ectomycorrhizas with Paxillus involutus enhance cadmium uptake and tolerance in Populus × canescens. Plant Cell Environ 37:627-642.
57. Mamashita T, Larocque GR, DesRochers A, Beaulieu J, Thomas BR, Mosseler A, Major J, Sidders D (2015) Short-term growth and morphological responses to nitrogen availability and plant density in hybrid poplars and willows. Biomass Bioenergy 81:88-97.
58. Massad TJ, Dyer LA, Vega CG (2012) Costs of defense and a test of the carbon-nutrient balance and growth-differentiation balance hypotheses for two co-occurring classes of plant defense. PLoS One 7:e47554. doi:10.1371/journal.pone.0047554
59. Nasholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31-48.
60. Novaes E, Osorio L, Drost DR et al. (2009) Quantitative genetic analysis of biomass and wood chemistry of Populus under different nitrogen levels. New Phytol 182:878-890.
61. Okamoto M, Tanaka Y, Abrams SR, Kamiya Y, Seki M, Nambara E (2009) High humidity induces abscisic acid 8′-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis. Plant Physiol 149:825-834.
62. Parkinson JA, Allen SE (1975) A wet oxidation procedure suitable for the determination of nitrogen and mineral nutrients in biological material. Commun Soil Sci Plant Anal 6:1-11.
63. Patterson K, Cakmak T, Cooper A, Lager I, Rasmusson AG, Escobar MA (2010) Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell Environ 33:1486-1501.
64. Peng M, Bi YM, Zhu T, Rothstein SJ (2007) Genome-wide analysis of Arabidopsis responsive transcriptome to nitrogen limitation and its regulation by the ubiquitin ligase gene NLA. Plant Mol Biol 65:775-797.
65. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36.
66. Pitre FE, Lafarguette F, Boyle B et al. (2010) High nitrogen fertilization and stem leaning have overlapping effects on wood formation in poplar but invoke largely distinct molecular pathways. Tree Physiol 30:1273-1289.
67. Plavcova L, Hacke UG, Almeida-Rodriguez AM, Li E, Douglas CJ (2013) Gene expression patterns underlying changes in xylem structure and function in response to increased nitrogen availability in hybrid poplar. Plant Cell Environ 36:186-199.
68. Polle A, Janz D, Teichmann T, Lipka V (2013) Poplar genetic engineering: promoting desirable wood characteristics and pest resistance. Appl Microbiol Biotechnol 97:5669-5679.
69. Provart N, Zhu T (2003) A browser-based functional classification SuperViewer for Arabidopsis genomics. Curr Comput Mol Biol 2003:271-272.
70. Rennenberg H, Dannenmann M, Gessler A, Kreuzwieser J, Simon J, Papen H (2009) Nitrogen balance in forest soils: nutritional limitation of plants under climate change stresses. Plant Biol 11:4-23.
71. Rennenberg H, Wildhagen H, Ehlting B (2010) Nitrogen nutrition of poplar trees. Plant Biol 12:275-291.
72. Reyes JC, Muro-Pastor MI, Florencio FJ (2004) The GATA family of transcription factors in Arabidopsis and rice. Plant Physiol 134:1718-1732.
73. Roberts K, Shirsat AH (2006) Increased extensin levels in Arabidopsis affect inflorescence stem thickening and height. J Exp Bot 57:537-545.
74. Robertson GP, Vitousek PM (2009) Nitrogen in agriculture: balancing the cost of an essential resource. Annu Rev Environ Resour 34:97-125.
75. Rueda-Lopez M, Crespillo R, Canovas FM, Avila C (2008) Differential regulation of two glutamine synthetase genes by a single Dof transcription factor. Plant J 56:73-85.
76. Ruffel S, Krouk G, Ristova D, Shasha D, Birnbaum KD, Coruzzi GM (2011) Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc Natl Acad Sci USA 108:18524-18529.
77. Ruzicka K, Strader LC, Bailly A et al. (2010) Arabidopsis PIS1 encodes the ABCG37 transporter of auxinic compounds including the auxin precursor indole-3-butyric acid. Proc Natl Acad Sci USA 107: 10749-10753.
78. Saito R, Smoot ME, Ono K, Ruscheinski J, Wang PL, Lotia S, Pico AR, Bader GD, Ideker T (2012) A travel guide to Cytoscape plugins. Nat Methods 9:1069-1076.
79. Schroder F, Lisso J, Lange P, Mussig C (2009) The extracellular EXO protein mediates cell expansion in Arabidopsis leaves. BMC Plant Biol 9:20. doi:10.1186/1471-2229-9-20
80. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498-2504.
81. Shi WG, Li H, Liu TX, Polle A, Peng CH, Luo ZB (2015) Exogenous abscisic acid alleviates zinc uptake and accumulation in Populus × canescens exposed to excess zinc. Plant Cell Environ 38:207-223.
82. Signora L, Smet ID, Foyer CH, Zhang H (2001) ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J 28:655-662.
83. Sun S, Wang H, Yu H, Zhong C, Zhang X, Peng J, Wang X (2013) GASA14 regulates leaf expansion and abiotic stress resistance by modulating reactive oxygen species accumulation. J Exp Bot 64:1637-1647.
84. Thimm O, Blasing O, Gibon Y et al. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914-939.
85. Tian Q, Chen F, Liu J, Zhang F, Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots. J Plant Physiol 165:942-951.
86. Tjaden G, Edwards JW, Coruzzi GM (1995) Cis elements and trans-acting factors affecting regulation of a nonphotosynthetic light-regulated gene for chloroplast glutamine synthetase. Plant Physiol 108: 1109-1117.
87. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111.
88. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511-515.
89. Turano FJ, Thakkar SS, Fang T, Weisemann JM (1997) Characterization and expression of NAD(H)-dependent glutamate dehydrogenase genes in Arabidopsis. Plant Physiol 113:1329-1341.
90. Vidal EA, Moyano TC, Riveras E, Contreras-Lopez O, Gutierrez RA (2013) Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. Proc Natl Acad Sci USA 110:12840-12845.
91. Walker-Simmons M (1987) ABA levels and sensitivity in developing wheat embryos of sprouting resistant and susceptible cultivars. Plant Physiol 84:61-66.
92. Walters D, Heil M (2007) Costs and trade-offs associated with induced resistance. Physiol Mol Plant Pathol 71:3-17.
93. Wang J, Chen L, Wang Y, Zhang J, Liang Y, Xu D (2013) A computational systems biology study for understanding salt tolerance mechanism in rice. PLoS One 8:e64929. doi:10.1371/journal.pone.0064929
94. Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136-138.
95. Wang R, Xing X, Crawford N (2007) Nitrite acts as a transcriptome signal at micromolar concentrations in Arabidopsis roots. Plant Physiol 145:1735-1745.
96. Wei H, Persson S, Mehta T, Srinivasasainagendra V, Chen L, Page GP, Somerville C, Loraine A (2006) Transcriptional coordination of the metabolic network in Arabidopsis. Plant Physiol 142:762-774.
97. Wei H, Yordanov Y, Kumari S, Georgieva T, Busov V (2013a) Genetic networks involved in poplar root response to low nitrogen. Plant Signal Behav 8:e27211. doi:10.4161/psb.27211
98. Wei H, Yordanov YS, Georgieva T, Li X, Busov V (2013b) Nitrogen deprivation promotes Populus root growth through global transcriptome reprogramming and activation of hierarchical genetic networks. New Phytol 200:483-497.
99. Xie Z, Zhang ZL, Zou X, Huang J, Ruas P, Thompson D, Shen QJ (2005) Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol 137:176-189.
100. Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153-182.
101. Yanagisawa S (2000) Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J 21:281-288.
102. Yanagisawa S, Schmidt RJ (1999) Diversity and similarity among recognition sequences of Dof transcription factors. Plant J 17:209-214.
103. Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508-514.
104. Yendrek CR, Lee YC, Morris V et al. (2010) A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula. Plant J 62:100-112.
105. Zhang H, Rong H, Pilbeam D (2007) Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. J Exp Bot 58:2329-2338.
106. Zhao Q, Zeng DH, Fan ZP (2010) Nitrogen and phosphorus transformations in the rhizospheres of three tree species in a nutrient-poor sandy soil. Appl Soil Ecol 46:341-346.