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Comparative Analysis of Differentially Expressed Genes in Rice Under Nitrogen and Phosphorus Starvation Stress Conditions

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Abstract

Nitrogen (N) and phosphorus (P) are two major mineral nutrients required for plant growth and development. Deficiencies in N or P results in both morphological and molecular changes such that plants develop adaptive responses to low N or P availability. In this study, we applied the Affymetrix Rice Genome array to analyze the overlap between the differentially expressed gene response to N and P starvation conditions. The results showed that a large number of genes were expressed differentially both under N starvation conditions and under P starvation conditions, including genes encoding a sulfate transporter, Fd-glutamate synthase, peroxidases, transcription factors, kinases and cytochrome P450s. In roots, 61, 42 and 159 genes were significantly up-regulated after 1 h, 24 h and 7 days, respectively, under both N and P starvation conditions, whereas 104, 50 and 166 genes, respectively, were significantly down-regulated. In shoots, 56, 104 and 101 genes were significantly up-regulated after 1 h, 24 h and 7 days, respectively, under both N and P starvation conditions, whereas 15, 80 and 59 genes, respectively, were significantly down-regulated. Generally, these differentially expressed genes belonged primarily to six biological process categories: molecular transport, molecular metabolism, regulation and modification, organism development, stress stimuli and electron transport. Our results may indicate some common physiological and genetic mechanisms in plant responses to environmental variations.

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References

  • Abel S, Nurnberger T, Ahnert V, Krauss GJ, Glund K (2000) Induction of an extracellular cyclic nucleotide phosphodiesterase as an accessory ribonucleolytic activity during phosphate starvation of cultured tomato cells. Plant Physiol 122:543–552

    Article  PubMed  CAS  Google Scholar 

  • Alexa A, Rahnenfuhrer J, Lengauer T (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22:1600–1607

    Article  PubMed  CAS  Google Scholar 

  • Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011

    Article  PubMed  CAS  Google Scholar 

  • Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 21:529–538

    Article  Google Scholar 

  • Bi Y-M, Wang RL, Zhu T, Rothstein SJ (2007) Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis. BMC Genomics 8:281–297

    Article  PubMed  Google Scholar 

  • Cai H, Xie W, Zhu T, Lian X (2012) Transcriptome response to phosphorus starvation in rice. Acta Physiol Plant 34:327–341

    Article  CAS  Google Scholar 

  • Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574

    Article  PubMed  CAS  Google Scholar 

  • Crawford NM, Forde BG (2002) Molecular and developmental biology of inorganic nitrogen nutrition. In: Meyerowitz E, Somerville C (eds) The arabidopsis book. American Society of Plant Biologists, Rockville, MD, http://www.aspb.org/publications/arabidopsis

  • del Pozo JC, Allona I, Rubio V, Leyva A, Pena A, Aragoncillo C, Paz-Ares J (1999) A type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilizing/oxidative stress conditions. Plant J 19:579–589

    Article  PubMed  Google Scholar 

  • Desikan R, Mackerness SAH, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172

    Article  PubMed  CAS  Google Scholar 

  • Diaz C, Saliba-Colombani V, Loudet O, Belluomo P, Moreau L, Daniel-Vedele F, Morot-Gaudry JF, Masclaux-Daubresse C (2006) Leaf yellowing and anthocyanin accumulation are two genetically independent strategies in response to nitrogen limitation in Arabidopsis thaliana. Plant Cell Physiol 47:74–83

    Article  PubMed  CAS  Google Scholar 

  • Ding L, Wang KJ, Jiang GM, Biswas DK, Xu H, Li LF, Li YH (2005) Effects of nitrogen deficiency on photosynthetic traits of maize hybrids released in different years. Ann Bot 96:925–930

    Article  PubMed  CAS  Google Scholar 

  • Duan K, Yi K, Dang L, Huang H, Wu W, Wu P (2008) Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant J 54:965–975

    Article  PubMed  CAS  Google Scholar 

  • Essigmann B, Güler S, Narang RA, Linke D, Benning C (1998) Phosphate availability affects the thylakoid lipid composition and expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 95:1950–1955

    Article  PubMed  CAS  Google Scholar 

  • Fang Z, Shao C, Meng Y, Wu P, Chen M (2009) Phosphate signaling in Arabidopsis and Oryza sativa. Plant Sci 176:170–180

    Article  CAS  Google Scholar 

  • Gan Y, Filleur S, Rahman A, Gotensparre S, Forde BG (2005) Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana. Planta 222:730–742

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez E, Solano R, Rubio V, Leyva A, Paz-Ares J (2005) Phosphate transporter traffic facilitator1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. Plant Cell 17:3500–3512

    Article  PubMed  CAS  Google Scholar 

  • Green PJ (1994) The ribonucleases of higher plants. Annu Rev Plant Physiol Plant Mol Biol 45:421–445

    Article  CAS  Google Scholar 

  • Gutiérrez RA, Lejay LV, Dean A, Chiaromonte F, Shasha DE, Coruzzi GM (2007) Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol 8:R7

    Article  PubMed  Google Scholar 

  • Gutierrez RA, Stokes TL, Thum K, Xu X, Obertello M, Katari MS, Tanurdzic M, Dean A, Nero DC, McClung CR, Coruzzi GM (2008) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc Natl Acad Sci USA 105:4939–4944

    Article  PubMed  CAS  Google Scholar 

  • Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May TM, Rahn C, Swarup R, Woolaway KE, White PJ (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 132:578–596

    Article  PubMed  CAS  Google Scholar 

  • Hammond JP, White PJ (2011) Sugar signaling in root responses to low phosphorus availability. Plant Physiol 156:1033–1040

    Article  PubMed  CAS  Google Scholar 

  • Hesse H, Nikiforova V, Gakiere B, Hoefgen R (2004) Molecular analysis and control of cysteine biosynthesis: integration of nitrogen and sulphur metabolism. J Exp Bot 55:1283–1292

    Article  PubMed  CAS  Google Scholar 

  • Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, Chory J (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22:2825–2827

    Article  PubMed  CAS  Google Scholar 

  • Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141

    Article  PubMed  CAS  Google Scholar 

  • Lam HM, Coschigano K, Oliveira IC, Melo-Oliveira R, Coruzzi G (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu Rev Plant Biol 47:569–593

    Article  CAS  Google Scholar 

  • Li L, Liu C, Lian X (2010) Gene expression profiles in rice roots under low phosphorus stress. Plant Mol Biol 72:423–432

    Article  PubMed  CAS  Google Scholar 

  • Li M, Qin C, Welti R, Wang X (2006) Double knockouts of phospholipases Dz1 and Dz2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol 140:761–770

    Article  PubMed  CAS  Google Scholar 

  • Lian X, Wang S, Zhang J, Feng Q, Zhang L, Fan D, Li X, Yuan D, Han B, Zhang Q (2006) Expression profiles of 10,422 genes at early stage of low nitrogen stress in rice assayed using a cDNA microarray. Plant Mol Biol 60:617–631

    Article  PubMed  CAS  Google Scholar 

  • Mahalingam R, Gomez-Buitrago AM, Eckardt N, Shah N, Guevara-Garcia A, Day P, Raina R, Fedoroff NV (2003) Characterizing the stress/defense transcriptome of Arabidopsis. Genome Biol 4:R20

    Article  PubMed  Google Scholar 

  • Malboobi MA, Lefebvre DD (1997) A phosphate-starvation inducible-glucosidase (psr3.2) isolated from Arabidopsis thaliana is a member of a distinct subfamily of the BGA family. Plant Mol Biol 34:57–68

    Article  PubMed  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic, San Diego

    Google Scholar 

  • Meunier B, de Visser SP, Shaik S (2004) Mechanism of oxidation reactions catalyzed by cytochrome P450 enzymes. Chem Rev 104:3947–3980

    Article  PubMed  CAS  Google Scholar 

  • 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 (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102:11934–11939

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun DJ, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102:7760–7765

    Article  PubMed  CAS  Google Scholar 

  • Miyake K, Ito T, Senda M, Ishikawa R, Harada T, Niizeki M, Akada S (2003) Isolation of a subfamily of genes for R2R3-MYB transcription factors showing up-regulated expression under nitrogen nutrient-limited conditions. Plant Mol Biol 53:237–245

    Article  PubMed  CAS  Google Scholar 

  • Muller R, Morant M, Jarmer H, Nilsson L, Nielsen TH (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143:156–171

    Article  PubMed  CAS  Google Scholar 

  • Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35:D883–D887

    Article  PubMed  CAS  Google Scholar 

  • Palenchar PM, Kouranov A, Lejay LV, Coruzzi GM (2004) Genome-wide patterns of carbon and nitrogen regulation of gene expression validate the combined carbon and nitrogen (CN)-signaling hypothesis in plants. Genome Biol 5:R91

    Article  PubMed  Google Scholar 

  • Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ (2007) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts Arabidopsis adaptability to nitrogen limitation. Plant J 50:320–337

    Article  PubMed  CAS  Google Scholar 

  • Prosser I, Purves J, Saker L, Clarkson D (2001) Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate. J Exp Bot 52:113–121

    Article  PubMed  CAS  Google Scholar 

  • Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693

    Article  PubMed  CAS  Google Scholar 

  • Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–719

    PubMed  CAS  Google Scholar 

  • Rubio V, Francisco L, Roberto S, Ana C, Martin JI, Antonio L, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular. Genes Dev 15:2122–2133

    Article  PubMed  CAS  Google Scholar 

  • Sano H, Youssefian S (1994) Light and nutritional regulation of transcripts encoding a wheat protein kinase homolog is mediated by cytokinins. Proc Natl Acad Sci USA 91:2582–2586

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Physiol 58:47–69

    CAS  Google Scholar 

  • Scheible WR, Gonzalez-Fontes A, Lauerer M, Muller-Rober B, Caboche M, Stitt M (1997) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–798

    PubMed  CAS  Google Scholar 

  • Scheible W-R, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, celluar growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483–2499

    Article  PubMed  CAS  Google Scholar 

  • Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832

    Article  PubMed  CAS  Google Scholar 

  • Sitt M, Muller C, Matt P, Gibon Y, Carillo P, Morcuende R, Scheible WR, Krapp A (2002) Steps towards an integrated view of nitrogen metabolism. J Exp Bot 53:959–970

    Article  Google Scholar 

  • Skopelitis DS, Paranychianakis NV, Kouvarakis A, Spyros A, Stephanou EG, Roubelakis-Angelakis KA (2007) The isoenzyme 7 of tobacco NAD(H)-dependent glutamate dehydrogenase exhibits high deaminating and low aminating activities in vivo. Plant Physiol 145:1726–1734

    Article  PubMed  CAS  Google Scholar 

  • Theodoru ME, Plaxton WC (1993) Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol 101:339–344

    Google Scholar 

  • Todd CD, Zeng P, Huete AM, Hoyos ME, Polacco JC (2004) Transcripts of MYB-like genes respond to phosphorus and nitrogen deprivation in Arabidopsis. Planta 219:1003–1009

    Article  PubMed  CAS  Google Scholar 

  • Wang R, Guegler K, La Brie ST, Crawford NM (2000) Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes that are induced by nitrate. Plant Cell 12:1491–1510

    PubMed  CAS  Google Scholar 

  • Wang R, Okamoto M, Xing X, Crawford NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol 132:556–567

    Article  PubMed  CAS  Google Scholar 

  • Wang S, Jiang J, Li T, Li H, Wang C, Wang Y, Liu G (2011) Influence of nitrogen, phosphorus, and potassium fertilization on flowering and expression of flowering-associated genes in white birch (Betula platyphylla Suk.). Plant Mol Biol Rep 29:794–801

    Article  CAS  Google Scholar 

  • Wang X (2005) Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiol 139:566–573

    Article  PubMed  CAS  Google Scholar 

  • Wang YH, Garvin DF, Kochian LV (2001) Nitrate-induced genes in tomato roots. Array analysis reveals novel genes that may play a role in nitrogen nutrition. Plant Physiol 127:345–359

    Article  PubMed  CAS  Google Scholar 

  • Wang YH, Garvin DF, Kochian LV (2002) Rapid induction of regulatory and transporter genes in response to phosphorus, potassium and iron deficiencies in tomato roots. Evidence for cross talk and root/rhizosphere-mediated signals. Plant Physiol 130:1361–1370

    Article  PubMed  CAS  Google Scholar 

  • Wasaki J, Yonetani R, Kuroda S, Shinano T, Yazaki J, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, Kishimoto N, Kikuchi S, Yamagishi M, Osaki M (2003) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ 26:1515–1523

    Article  CAS  Google Scholar 

  • Werck-Reichhart D, Feyereisen R (2000) Cytochromes P450: a success story. Genome Biol 1(6):3003.1–3003.9

    Article  Google Scholar 

  • Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, Deng XW (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132:1260–1271

    Article  PubMed  CAS  Google Scholar 

  • Wu ZJ, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F (2004) A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99:909–917

    Article  Google Scholar 

  • Xu H, He X, Wang K, Chen L, Li K (2012) Identification of early nitrate stress response genes in spinach roots by suppression subtractive hybridization. Plant Mol Biol Rep 30:633–642

    Article  CAS  Google Scholar 

  • Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T (2004) Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl Acad Sci USA 101:7833–7838

    Article  PubMed  CAS  Google Scholar 

  • Yoshida S, Forno DA, Cook JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. International Rice Research Institute, Manila

    Google Scholar 

  • Yu S, Zhang F, Yu Y, Zhang D, Zhao X, Wang W (2012) Transcriptome profiling of dehydration stress in the Chinese cabbage (Brassica rapa L. ssp. pekinensis) by tag sequencing. Plant Mol Biol Rep 30:17–28

    Article  CAS  Google Scholar 

  • Yuan H, Liu D (2008) Signaling components involved in plant responses to phosphate starvation. J Integr Plant Biol 50:849–859

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported in part by grants from the National Natural Science Foundation of China (31000932); the Special Fund for Agro-scientific Research in the Public Interest (201003016); the Specialized Research Found for the Doctoral Program of Higher Education, the Ministry of Education of China (20100146120017).

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Correspondence to Hongmei Cai.

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Supplementary Fig. S1a,b

Clustering analysis of rice genes that exhibited differential expression in response to N or P starvation at three time points examined in either roots or shoots. a Comparative analysis of differentially expressed genes in roots at 1 h (NR1-CR1), 24 h (NR2-CR2) and 7 days (NR3-CR3) after N starvation and at 1 h (PR1-CR1), 24 h (PR2-CR2) and 7 days (PR3-CR3) after P starvation; b Comparative analysis of differentially expressed genes in shoots at 1 h (NS1-CS1), 24 h (NS2-CS2) and 7 days (NS3-CS3) after N starvation and at 1 h (PS1-CS1), 24 h (PS2-CS2) and 7 days (PS3-CS3) after P starvation. (JPEG 384 kb)

High resolution image (TIFF 548 kb)

Supplementary Fig. S2

Heatmap of gene ontology (GO) enrichment analyses at 1 h, 24 h and 7 days in roots (NR) and shoots (NS) under N starvation and in roots (PR) and shoots (PS) under P starvation. Significant GO categories were identified using the weight FET method (P-value < 0.05) in the topGO package and categories higher than level six (based on the GO tree structure) were selected. Then, the P-values of the GO categories were transformed to base 10 logarithms. The logarithm was reversed to minus if the GO category was significantly down-regulated. The up-regulated GO category is denoted in magenta, while down-regulated is denoted in blue. GO categories significant in both the up-regulated and down-regulated direction are not displayed in this figure. (JPEG 775 kb)

High resolution image (TIFF 1351 kb)

Supplementary Table S1

GO enrichments both for N (-N) and P (-P) starvation after 1 h treatment. (DOC 175 kb)

Supplementary Table S2

GO enrichments both for N (-N) and P (-P) starvation after 24 h treatment. (DOC 73 kb)

Supplementary Table S3

GO enrichments both for N (−N) and P (−P) starvation after 7 days treatment. (DOC 173 kb)

Supplementary Table S4

GO enrichments for N starvation only after 1 h treatment. (DOC 268 kb)

Supplementary Table S5

GO enrichments for N starvation only after 24 h treatment. (DOC 212 kb)

Supplementary Table S6

GO enrichments for N starvation only after 7 days treatment. (DOC 250 kb)

Supplementary Table S7

GO enrichments for P starvation only after 1 h treatment. (DOC 126 kb)

Supplementary Table S8

GO enrichments for P starvation only after 24 h treatment. (DOC 146 kb)

Supplementary Table S9

GO enrichments for P starvation only after 7 day treatment. (DOC 167 kb)

Supplementary Table S10

Significantly changed genes related to molecular transport under N starvation (−N) and P starvation (−P) conditions. (DOC 218 kb)

Supplementary Table S11

Significantly changed genes involved in molecular metabolism under N starvation (−N) and P starvation (−P) conditions. (DOC 547 kb)

Supplementary Table S12

Significantly changed genes involved in regulation and modification under N starvation (−N) and P starvation (−P) conditions. (DOC 856 kb)

Supplementary Table S13

Significantly changed genes related to organism development under N starvation (−N) and P starvation (−P) conditions. (DOC 243 kb)

Supplementary Table S14

Significantly changed genes response to stress stimuli under N starvation (−N) and P starvation (−P) conditions. (DOC 363 kb)

Supplementary Table S15

Significantly changed genes related to electron transport under N starvation (−N) and P starvation (−P) conditions. (DOC 304 kb)

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Cai, H., Xie, W. & Lian, X. Comparative Analysis of Differentially Expressed Genes in Rice Under Nitrogen and Phosphorus Starvation Stress Conditions. Plant Mol Biol Rep 31, 160–173 (2013). https://doi.org/10.1007/s11105-012-0485-8

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