Abstract
The present study aimed to delineate the genes mediating nitrogen metabolism in cucumber (Cucumis sativus L.) and elucidate the mechanisms underlying the response to long-term nitrogen limitation. As an economically important crop, cucumber is strongly nitrogen dependent. The mechanisms underlying nitrogen metabolism in cucumber are not fully known. This study found that cucumber developed to a 3.5-leaf stage with reduced plant size and biomass under chronic low nitrogen stress condition. Gene expression profiling and analysis of cucumber roots and leaves under nitrogen-starved condition identified a total of 2991 unigenes as reliable differentially expressed genes (DEGs). A comprehensive analysis of the transcriptome revealed that the mechanisms underlying the response of cucumber roots to nitrogen-deficient stress were considerably different from those of its leaves. Importantly, the DEGs involved in the photosynthesis were almost downregulated, suggesting that the photosystem was sensitive to nitrogen starvation. Otherwise, the nitrate metabolic pathway of cucumber was suppressed by nitrogen deficiency, which was further confirmed by quantitative reverse transcription–polymerase chain reaction. This study represents a comparative analysis of the transcriptome levels of roots and leaves of cucumber, which possibly provides a valuable resource for further investigating the mechanism underlying plant response to long-term nitrogen limitation stress along with the candidate genes controlling the nitrogen metabolism.
Similar content being viewed by others
References
Beatty PH, Shrawat AK, Carroll RT, Zhu T, Good AG (2009) Transcriptome analysis of nitrogen-efficient rice over-expressing alanine aminotransferase. Plant Biotechnol J 7(6):562–576
Bi YM, 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 Genom 8:281
Bouguyon E, Brun F, Meynard D, Kubeš M, Pervent M, LeranS Lacombe B, Krouk G, Guiderdoni E, Zažímalová E, Hoyerová K, Nacry P, Gojon A (2015) Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat Plants 1:15015
Chen R, Tian M, Wu X, Huang Y (2011) Differential global gene expression changes in response to low nitrogen stress in two maize inbred lines with contrasting low nitrogen tolerance. Genes Genom 33:491–497
DeBolt S, Scheible WR, Schrick K, Auer M, Beisson F, Bischoff V, Bouvier-Navé P, Carroll A, Hematy K, Li Y, Milne J, Nair M, Schaller H, Zemla M, Somerville C (2009) Mutations in UDP-glucose: sterol glucosyltransferase in Arabidopsis cause transparent testa phenotype and suberization defect in seeds. Plant Physiol 151:78–87
Guo T, Xuan H, Yang Y, Wang L, Wei L, Wang Y, Kang G (2014) Transcription analysis of genes encoding the wheat root transporter NRT1 and NRT2 families during nitrogen starvation. J Plant Growth Regul 3(4):837–848
Hu B, Wang W, Ou S, Tang J, Li H, Che R, Zhang Z, Chai X, Wang H, Wang Y, Liang C, Liu L, Piao Z, Deng Q, Deng K, Xu C, Liang Y, Zhang L, Li L, Chu C (2015) Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. Nat Genet 47:834–838
Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P, Ren Y, Zhu H, Jun Li, Lin K, Jin W, Fei Z, Li G, Staub J, Kilian A, van der Vossen EAG, Wu Y, Guo J, He J, Jia Z, Ren Y, Tian G, Lu Y, Ruan J, Qian W, Wang M, Huang Q, Li B, Xuan Z, Cao J, Asan WuZ, Zhang J, Cai Q, Bai Y, Zhao B, Han Y, Li Y, Li X, Wang S, Shi Q, Liu S, Cho WK, Kim J, Xu Y, Heller-Uszynska K, Miao H, Cheng Z, Zhang S, Wu J, Yang Y, Kang H, Li M, Liang H, Ren X, Shi Z, Wen M, Jian M, Yang H, Zhang G, Yang Z, Chen R, Liu S, Li J, Ma L, Liu H, Zhou Y, Zhao J, Fang X, Li G, Fang L, Li Y, Liu D, Zheng H, Zhang Y, Qin N, Li Z, Yang G, Yang S, Bolund L, Kristiansen K, Zheng H, Li S, Zhang X, Yang H, Wang J, Sun R, Zhang B, Jiang S, Wang J, Du Y, Li S (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41(12):1275–1281
Krapp A, Berthomé R, Orsel M, Mercey-Boutet S, Yu A, Castaings L, Elftieh S, Major H, Renou JP, Daniel-Vedele F (2011) Arabidopsis roots and shoots show distinct temporal adaptation patterns toward nitrogen starvation. Plant Physiol 157:1255–1282
Kurai T, Wakayama M, Abiko T, Yanagisawa S, Aoki N, Ohsugi R (2011) Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low nitrogen conditions. Plant Biotechnol J 9:826–837
Lejay L, Wirth J, Pervent M, Cross JM, Tillard P, Gojon A (2008) Oxidative pentose phosphate pathway-dependent sugar sensing as a mechanism for regulation of root ion transporters by photosynthesis. Plant Physiol 146(4):2036–2053
Lin SH, Kuo HF, Canivence G, Lin CS, Lepetit M, Hsu PK (2008) Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell 20(9):2514–2528
Lin W, Hagen E, Fulcher A, Hren MT, Cheng ZM (2013) Overexpressing the ZmDof1 gene in Populus does not improve growth and nitrogen assimilation under low-nitrogen conditions. Plant Cell Tissue Organ Cult 113(1):51–61
Loqué D, Yuan L, Yang L, Kojima S, Kojima S, Gojon A, Wirth J, Gazzarrini S, Ishiyama K, Takahashi H, Wirén N (2006) A nitrogen-dependent additive contribution of AtAMT1;1 and AtAMT1;3 to ammonium uptake across the plasma membrane of Arabidopsis roots. Plant J 48:522–534
Masclaux-Daubresse C, Chardon F (2011) Exploring nitrogen remobilization for seed filling using natural variation in Arabidopsis thaliana. J Exp Bot 62:2131–2142
Migocka M, Warzybok A, Kłobus G (2013) The genomic organization and transcriptional pattern of genes encoding nitrate transporters 1 (NRT1) in cucumber. Plant Soil 364:245–260
Miller AJ, Fan X, Orsel M, Smith MJ, Wells DM (2007) Nitrate transport and signaling. J Exp Bot 58:2297–2306
Parker JL, Newstead S (2014) Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507:68–72
Paul M, Driscoll S (2008) Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source: sink imbalance. Plant Cell Environ 20:110–116
Reid JB, Trolove SN, Tan Y, Johnstone PR (2016) Nitrogen or potassium preconditioning affects uptake of both nitrate and potassium in young wheat (Triticum aestivum). Ann Appl Biol 168(1):66–80
Sindelar AJ, Sheaffer CC, Lamb JA, Jung HJG, Rosen CJ (2015) Maize stover and cob cell wall composition and ethanol potential as affected by nitrogen fertilization. Bioenergy Res 8:1352–1361
Tattini M, Loreto F, Fini A, Guidi L, Brunetti C, Velikova V, Gori A, Ferrini F (2015) Isoprenoids and phenylpropanoids are part of the antioxidant defense orchestrated daily by drought-stressed Platanus × acerifolia plants during Mediterranean summers. New Phytol 207(3):613–626
Wang WG, Li R, Liu B, Li L, Wang SH, Chen F (2011) Effects of low nitrogen and drought stresses on proline synthesis of Jatropha curcas seedling. Acta Physiol Plant 33:1591–1595
Welch LF, Boone LV, Chambliss CG, Christiansen AT, Mulvaney DL, Oldham MG, Pendleton JW (1973) Soybean yields with direct and residual nitrogen fertilization. Agron J 65(4):547–550
Wu T, Qin Z, Fan L, Xue C, Zhou X, Xin M, Du Y (2014) Involvement of CsNRT1.7 in nitrate recycling during senescence in cucumber. Plant Nutr Soil Sci 177(5):714–721
Xue LJ, Guo W, Yuan Y, Anino EO, Nyamdari B, Wilson MC, Frost CJ, Chen HY, Babst BA, Harding SA, Tsai CJ (2013) Constitutively elevated salicylic acid levels alter photosynthesis and oxidative state but not growth in transgenic populus. Plant Cell 25(7):2714–2730
Yang H, Xu L, Cui H, Zhong B, Liu G, Shi H (2013) Low nitrogen-induced expression of cyclophilin in Nicotiana tabacum. J Plant Res 126:121–129
Yu Y, Zhen S, Wang S, Wang Y, Cao H, Zhang Y, Li Y, Yan Y (2016) Comparative transcriptome analysis of wheat embryo and endosperm responses to ABA and H2O2 stresses during seed germination. BMC Genom 17(1):1–18
Yuan L, Loqué D, Kojima S, Rauch S, Ishiyama K, Inoue E, Takahashi H, von Wirén N (2007) The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. Plant Cell 19(8):2636–2652
Zhao W, Yang X, Yu H, Jiang W, Sun N, Liu X, Liu X, Zhang X, Wang Y, Gu X (2015) RNA-Seq-based transcriptome profiling of early nitrogen deficiency response in cucumber seedlings provides new insight into the putative nitrogen regulatory network. Plant Cell Physiol 56(3):455–467
Acknowledgements
This study was funded by the National Natural Science Foundation of China (31401863), Young University Innovative Talent Training Program of Heilongjiang Province (UNPYSCT-2016007), Supporting Certificate of Heilongjiang Postdoctoral Scientific Research Developmental Fund (LBH-Q16021), the Open Project of Heilongjiang Provincial Key University Laboratory of Cold Area Vegetable Biology (CVB2012-001), Certificate of China Postdoctoral Science Foundation (2013M540265) and Certificate of Heilongjiang Postdoctoral Fund (LBH-Z12037). And there are no financial competing interests.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Communicated by T. K. Mondal.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xin, M., Wang, L., Liu, Y. et al. Transcriptome profiling of cucumber genome expression in response to long-term low nitrogen stress. Acta Physiol Plant 39, 130 (2017). https://doi.org/10.1007/s11738-017-2429-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-017-2429-2