Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Physiological and transcriptome analysis of Dendrobium officinale under low nitrogen stress

Hangtao Wu A § , Jin Li A § , Qian Pu A , Chunyi Mi A , Guohong Zeng A , Ying Chen A , Dedong Kong B , Xiaorong Zuo C , Xiufang Hu https://orcid.org/0000-0002-8509-6763 A * and Ou Li https://orcid.org/0000-0002-5384-0463 A *
+ Author Affiliations
- Author Affiliations

A Zhejiang Province Key Laboratory of Plant Secondary Metabolism and Regulation, College of Life Science, Zhejiang Sci-Tech University, Hangzhou 310018, P.R. China.

B Institute of Digital Agriculture, Zhejiang Academy of Agricultural Sciences, Hangzhou 310018, P.R. China.

C Xi’an Ande Pharmaceutical Co., Ltd, Zhenping Branch, Xi’an 710000, P.R. China.

* Correspondence to: huxiuf@sina.com, ouli@zstu.edu.cn

Handling Editor: Ulrike Mathesius

Functional Plant Biology 50(4) 314-334 https://doi.org/10.1071/FP22061
Submitted: 1 April 2022  Accepted: 6 February 2023   Published: 6 March 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Nitrogen (N) is the main nutrient of plants, and low nitrogen usually affects plant growth and crop yield. The traditional Chinese herbal medicine Dendrobium officinale Kimura et. Migo is a typical low nitrogen-tolerant plant, and its mechanism in response to low nitrogen stress has not previously been reported. In this study, physiological measurements and RNA-Seq analysis were used to analyse the physiological changes and molecular responses of D. officinale under different nitrogen concentrations. The results showed that under low nitrogen levels, the growth, photosynthesis and superoxide dismutase activity were found to be significantly inhibited, while the activities of peroxidase and catalase, the content of polysaccharides and flavonoids significantly increased. Differentially expressed genes (DEGs) analysis showed that nitrogen and carbon metabolisms, transcriptional regulation, antioxidative stress, secondary metabolite synthesis and signal transduction all made a big difference in low nitrogen stress. Therefore, copious polysaccharide accumulation, efficient assimilation and recycling of nitrogen, as well as rich antioxidant components play critical roles. This study is helpful for understanding the response mechanism of D. officinale to low nitrogen levels, which might provide good guidance for practical production of high quality D. officinale.

Keywords: abiotic stress, Dendrobium officinale, flavonoids, low nitrogen stress, physiological, polysaccharides, responses to nitrogen treatment, transcriptomic.


References

Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.
Catalase in vitro.Crossref | GoogleScholarGoogle Scholar |

Alfaifi SA, Khan MA, Migdadi HM, Jakse J, Ammar MH, El-Harty EH, Althamrah MI, Afzal M, Javed MM, Alghamdi SS (2015) Analysis of ESTs from the date palm (Phoenix dactylifera L.) cv. Sukary, an elite variety. Plant Omics 8, 441–448.

Amtmann A, Armengaud P (2009) Effects of N, P, K and S on metabolism: new knowledge gained from multi-level analysis. Current Opinion in Plant Biology 12, 275–283.
Effects of N, P, K and S on metabolism: new knowledge gained from multi-level analysis.Crossref | GoogleScholarGoogle Scholar |

Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar |

Argueso CT, Ferreira FJ, Kieber JJ (2009) Environmental perception avenues: the interaction of cytokinin and environmental response pathways. Plant, Cell & Environment 32, 1147–1160.
Environmental perception avenues: the interaction of cytokinin and environmental response pathways.Crossref | GoogleScholarGoogle Scholar |

Asano T, Wakayama M, Aoki N, Komatsu S, Ichikawa H, Hirochika H, Ohsugi R (2010) Overexpression of a calcium-dependent protein kinase gene enhances growth of rice under low-nitrogen conditions. Plant Biotechnology 27, 369–373.
Overexpression of a calcium-dependent protein kinase gene enhances growth of rice under low-nitrogen conditions.Crossref | GoogleScholarGoogle Scholar |

Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44, 276–287.
Superoxide dismutase: improved assays and an assay applicable to acrylamide gels.Crossref | GoogleScholarGoogle Scholar |

Becker TW, Foyer C, Caboche M (1992) Light-regulated expression of the nitrate-reductase and nitrite-reductase genes in tomato and in the phytochrome-deficient aurea mutant of tomato. Planta 188, 39–47.
Light-regulated expression of the nitrate-reductase and nitrite-reductase genes in tomato and in the phytochrome-deficient aurea mutant of tomato.Crossref | GoogleScholarGoogle Scholar |

Bi Y-M, Wang R-L, 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
Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Bichsel RG, Starman TW, Wang Y-T (2008) Nitrogen, phosphorus, and potassium requirements for optimizing growth and flowering of the nobile Dendrobium as a potted orchid. HortScience 43, 328–332.
Nitrogen, phosphorus, and potassium requirements for optimizing growth and flowering of the nobile Dendrobium as a potted orchid.Crossref | GoogleScholarGoogle Scholar |

Boatright WL (2016) Oxygen dependency of one-electron reactions generating ascorbate radicals and hydrogen peroxide from ascorbic acid. Food Chemistry 196, 1361–1367.
Oxygen dependency of one-electron reactions generating ascorbate radicals and hydrogen peroxide from ascorbic acid.Crossref | GoogleScholarGoogle Scholar |

Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiology 114, 1–7.
Bioprotective alkaloids of grass-fungal endophyte symbioses.Crossref | GoogleScholarGoogle Scholar |

Castilhos G, Lazzarotto F, Spagnolo-Fonini L, Bodanese-Zanettini MH, Margis-Pinheiro M (2014) Possible roles of basic helix-loop-helix transcription factors in adaptation to drought. Plant Science 223, 1–7.
Possible roles of basic helix-loop-helix transcription factors in adaptation to drought.Crossref | GoogleScholarGoogle Scholar |

Chance B, Maehly AC (1955) Assay of catalase and peroxidases. Methods in Enzymology 2, 764–775.
Assay of catalase and peroxidases.Crossref | GoogleScholarGoogle Scholar |

Chen Z, Liu C, Wang Y, He T, Gao R, Xu H, Guo G, Li Y, Zhou L, Lu R, Huang J (2018) Expression analysis of nitrogen metabolism-related genes reveals differences in adaptation to low-nitrogen stress between two different barley cultivars at seedling stage. International Journal of Genomics 2018, 8152860
Expression analysis of nitrogen metabolism-related genes reveals differences in adaptation to low-nitrogen stress between two different barley cultivars at seedling stage.Crossref | GoogleScholarGoogle Scholar |

Chen F, Huang G, Yang Z, Hou Y (2019) Antioxidant activity of Momordica charantia polysaccharide and its derivatives. International Journal of Biological Macromolecules 138, 673–680.
Antioxidant activity of Momordica charantia polysaccharide and its derivatives.Crossref | GoogleScholarGoogle Scholar |

Chen H, Liu Y, Zhang J, Chen Y, Dai C, Tian R, Liu T, Chen M, Yang G, Wang Z, Li H, Cao X, Gao X (2022) Amino acid transporter gene TaATLa1 from Triticum aestivum L. improves growth under nitrogen sufficiency and is down regulated under nitrogen deficiency. Planta 256, 65
Amino acid transporter gene TaATLa1 from Triticum aestivum L. improves growth under nitrogen sufficiency and is down regulated under nitrogen deficiency.Crossref | GoogleScholarGoogle Scholar |

Chomchan R, Siripongvutikorn S, Puttarak P, Rattanapon R (2016) Investigation of phytochemical constituents, phenolic profiles and antioxidant activities of ricegrass juice compared to wheatgrass juice. Functional Foods in Health and Disease 6, 822–835.
Investigation of phytochemical constituents, phenolic profiles and antioxidant activities of ricegrass juice compared to wheatgrass juice.Crossref | GoogleScholarGoogle Scholar |

Chun L, Mi G, Li J, Chen F, Zhang F (2005) Genetic analysis of maize root characteristics in response to low nitrogen stress. Plant and Soil 276, 369–382.
Genetic analysis of maize root characteristics in response to low nitrogen stress.Crossref | GoogleScholarGoogle Scholar |

Crawford NM, Glass ADM (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends in Plant Science 3, 389–395.
Molecular and physiological aspects of nitrate uptake in plants.Crossref | GoogleScholarGoogle Scholar |

Cui C, Zhang S, You L, Ren J, Luo W, Chen W, Zhao M (2013) Antioxidant capacity of anthocyanins from Rhodomyrtus tomentosa (Ait.) and identification of the major anthocyanins. Food Chemistry 139, 1–8.
Antioxidant capacity of anthocyanins from Rhodomyrtus tomentosa (Ait.) and identification of the major anthocyanins.Crossref | GoogleScholarGoogle Scholar |

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

Fini A, Brunetti C, Di Ferdinando M, Ferrini F, Tattini M (2011) Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants. Plant Signaling & Behavior 6, 709–711.
Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants.Crossref | GoogleScholarGoogle Scholar |

Forde BG (2000) Nitrate transporters in plants: structure, function and regulation. Biochimica et Biophysica Acta (BBA) - Biomembranes 1465, 219–235.
Nitrate transporters in plants: structure, function and regulation.Crossref | GoogleScholarGoogle Scholar |

Frink CR, Waggoner PE, Ausubel JH (1999) Nitrogen fertilizer: retrospect and prospect. Proceedings of the National Academy of Sciences of the United States of America 96, 1175–1180.
Nitrogen fertilizer: retrospect and prospect.Crossref | GoogleScholarGoogle Scholar |

Gill SS, Anjum NA, Gill R, Yadav S, Hasanuzzaman M, Fujita M, Mishra P, Sabat SC, Tuteja N (2015) Superoxide dismutase–mentor of abiotic stress tolerance in crop plants. Environmental Science and Pollution Research 22, 10375–10394.
Superoxide dismutase–mentor of abiotic stress tolerance in crop plants.Crossref | GoogleScholarGoogle Scholar |

Glevarec G, Bouton S, Jaspard E, Riou M-T, Cliquet J-B, Suzuki A, Limami AM (2004) Respective roles of the glutamine synthetase/glutamate synthase cycle and glutamate dehydrogenase in ammonium and amino acid metabolism during germination and post-germinative growth in the model legume Medicago truncatula. Planta 219, 286–297.
Respective roles of the glutamine synthetase/glutamate synthase cycle and glutamate dehydrogenase in ammonium and amino acid metabolism during germination and post-germinative growth in the model legume Medicago truncatula.Crossref | GoogleScholarGoogle Scholar |

Grossman A, Takahashi H (2001) Macronutrient utilization by photosynthetic eukaryotes and the fabric of interactions. Annual Review of Plant Physiology and Plant Molecular Biology 52, 163–210.
Macronutrient utilization by photosynthetic eukaryotes and the fabric of interactions.Crossref | GoogleScholarGoogle Scholar |

Gu DY, Wang XF, Gao JJ, Jiao J, Liu ZL, Zhang YY (2018) Effects of purified humic acid on the growth and nitrogen metabolism of cucumber seedlings under nitrogen stress. The Journal of Applied Ecology 29, 2575–2582.
Effects of purified humic acid on the growth and nitrogen metabolism of cucumber seedlings under nitrogen stress.Crossref | GoogleScholarGoogle Scholar |

Halliday KJ, Martínez-Garcia JF, Josse E-M (2009) Integration of light and auxin signaling. Cold Spring Harbor Perspectives in Biology 1, a001586
Integration of light and auxin signaling.Crossref | GoogleScholarGoogle Scholar |

Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42–52.
The protein kinase family: conserved features and deduced phylogeny of the catalytic domains.Crossref | GoogleScholarGoogle Scholar |

Hara M, Fujinaga M, Kuboi T (2004) Radical scavenging activity and oxidative modification of citrus dehydrin. Plant Physiology and Biochemistry 42, 657–662.
Radical scavenging activity and oxidative modification of citrus dehydrin.Crossref | GoogleScholarGoogle Scholar |

Harmon AC, Gribskov M, Harper JF (2000) CDPKs – a kinase for every Ca2+ signal? Trends in Plant Science 5, 154–159.
CDPKs – a kinase for every Ca2+ signal?Crossref | GoogleScholarGoogle Scholar |

He C, Zhang J, Liu X, Zeng S, Wu K, Yu Z, Wang X, Teixeira da Silva JA, Lin Z, Duan J (2015) Identification of genes involved in biosynthesis of mannan polysaccharides in Dendrobium officinale by RNA-seq analysis. Plant Molecular Biology 88, 219–231.
Identification of genes involved in biosynthesis of mannan polysaccharides in Dendrobium officinale by RNA-seq analysis.Crossref | GoogleScholarGoogle Scholar |

Ho C-H, Lin S-H, Hu H-C, Tsay Y-F (2009) CHL1 functions as a nitrate sensor in plants. Cell 138, 1184–1194.
CHL1 functions as a nitrate sensor in plants.Crossref | GoogleScholarGoogle Scholar |

Huang W, Xue A, Niu H, Jia Z, Wang J (2009) Optimised ultrasonic-assisted extraction of flavonoids from Folium eucommiae and evaluation of antioxidant activity in multi-test systems in vitro. Food Chemistry 114, 1147–1154.
Optimised ultrasonic-assisted extraction of flavonoids from Folium eucommiae and evaluation of antioxidant activity in multi-test systems in vitro.Crossref | GoogleScholarGoogle Scholar |

Huang G, Mei X, Hu J (2017) The antioxidant activities of natural polysaccharides. Current Drug Targets 18, 1296–1300.
The antioxidant activities of natural polysaccharides.Crossref | GoogleScholarGoogle Scholar |

Hunter T, Karin M (1992) The regulation of transcription by phosphorylation. Cell 70, 375–387.
The regulation of transcription by phosphorylation.Crossref | GoogleScholarGoogle Scholar |

Ibrahim MH, Jaafar HZE, Rahmat A, Rahman ZA (2012) Involvement of nitrogen on flavonoids, glutathione, anthocyanin, ascorbic acid and antioxidant activities of Malaysian medicinal plant Labisia pumila Blume (Kacip Fatimah). International Journal of Molecular Sciences 13, 393–408.
Involvement of nitrogen on flavonoids, glutathione, anthocyanin, ascorbic acid and antioxidant activities of Malaysian medicinal plant Labisia pumila Blume (Kacip Fatimah).Crossref | GoogleScholarGoogle Scholar |

Jaffar MA, Song A, Faheem M, Chen S, Jiang J, Liu C, Fan Q, Chen F (2016) Involvement of CmWRKY10 in drought tolerance of chrysanthemum through the ABA-signaling pathway. International Journal of Molecular Sciences 17, 693
Involvement of CmWRKY10 in drought tolerance of chrysanthemum through the ABA-signaling pathway.Crossref | GoogleScholarGoogle Scholar |

Jiang Y, Duan Y, Yin J, Ye S, Zhu J, Zhang F, Lu W, Fan D, Luo K (2014) Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. Journal of Experimental Botany 65, 6629–6644.
Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses.Crossref | GoogleScholarGoogle Scholar |

Karuppanapandian T, Wang HW, Prabakaran N, Jeyalakshmi K, Kwon M, Manoharan K, Kim W (2011) 2,4-dichlorophenoxyacetic acid-induced leaf senescence in mung bean (Vigna radiata L. Wilczek) and senescence inhibition by co-treatment with silver nanoparticles. Plant Physiology and Biochemistry 49, 168–177.
2,4-dichlorophenoxyacetic acid-induced leaf senescence in mung bean (Vigna radiata L. Wilczek) and senescence inhibition by co-treatment with silver nanoparticles.Crossref | GoogleScholarGoogle Scholar |

Kudla J, Xu Q, Harter K, Gruissem W, Luan S (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proceedings of the National Academy of Sciences of the United States of America 96, 4718–4723.
Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals.Crossref | GoogleScholarGoogle Scholar |

Landi M, Guidi L, Pardossi A, Tattini M, Gould KS (2014) Photoprotection by foliar anthocyanins mitigates effects of boron toxicity in sweet basil (Ocimum basilicum). Planta 240, 941–953.
Photoprotection by foliar anthocyanins mitigates effects of boron toxicity in sweet basil (Ocimum basilicum).Crossref | GoogleScholarGoogle Scholar |

Lea US, Slimestad R, Smedvig P, Lillo C (2007) Nitrogen deficiency enhances expression of specific MYB and bHLH transcription factors and accumulation of end products in the flavonoid pathway. Planta 225, 1245–1253.
Nitrogen deficiency enhances expression of specific MYB and bHLH transcription factors and accumulation of end products in the flavonoid pathway.Crossref | GoogleScholarGoogle Scholar |

Li M, Hirata Y, Xu G, Niwa M (1990) Determination of polysaccharide contents in the drugs of Dendrobium. Chinese Traditional and Herbal Drugs 21, 10–12.

Li O, Li A, Zhang C, Huang J, Meng Y, Yuan S, Huang J, Gao X, Yao Y, Yin R, Hu J, Ding B, Hu X (2018) Identification and characterization of six glycosyltransferases involved in the biosynthesis of a new bacterial exopolysaccharide in Paenibacillus elgii. Applied Microbiology and Biotechnology 102, 1357–1366.
Identification and characterization of six glycosyltransferases involved in the biosynthesis of a new bacterial exopolysaccharide in Paenibacillus elgii.Crossref | GoogleScholarGoogle Scholar |

Li Z, Jiang H, Yan H, Jiang X, Ma Y, Qin Y (2021) Carbon and nitrogen metabolism under nitrogen variation affects flavonoid accumulation in the leaves of Coreopsis tinctoria. PeerJ 9, e12152
Carbon and nitrogen metabolism under nitrogen variation affects flavonoid accumulation in the leaves of Coreopsis tinctoria.Crossref | GoogleScholarGoogle 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 10422 genes at early stage of low nitrogen stress in rice assayed using a cDNA microarray. Plant Molecular Biology 60, 617–631.
Expression profiles of 10422 genes at early stage of low nitrogen stress in rice assayed using a cDNA microarray.Crossref | GoogleScholarGoogle Scholar |

Liang J, He J (2018) Protective role of anthocyanins in plants under low nitrogen stress. Biochemical and Biophysical Research Communications 498, 946–953.
Protective role of anthocyanins in plants under low nitrogen stress.Crossref | GoogleScholarGoogle Scholar |

Liang T, Yuan Z, Fu L, Zhu M, Luo X, Xu W, Yuan H, Zhu R, Hu Z, Wu X (2021) Integrative transcriptomic and proteomic analysis reveals an alternative molecular network of glutamine synthetase 2 corresponding to nitrogen deficiency in rice (Oryza sativa L.). International Journal of Molecular Sciences 22, 7674
Integrative transcriptomic and proteomic analysis reveals an alternative molecular network of glutamine synthetase 2 corresponding to nitrogen deficiency in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar |

Livingston DP, Hincha DK, Heyer AG (2009) Fructan and its relationship to abiotic stress tolerance in plants. Cellular and Molecular Life Sciences 66, 2007–2023.
Fructan and its relationship to abiotic stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar |

Luo Q-L, Tang Z-H, Zhang X-F, Zhong Y-H, Yao S-Z, Wang L-S, Lin C-W, Luo X (2016) Chemical properties and antioxidant activity of a water-soluble polysaccharide from Dendrobium officinale. International Journal of Biological Macromolecules 89, 219–227.
Chemical properties and antioxidant activity of a water-soluble polysaccharide from Dendrobium officinale.Crossref | GoogleScholarGoogle Scholar |

Miflin BJ, Lea PJ (1980) Ammonia assimilation. In ‘The Biochemistry of plants’. Amino acid and their derivatives. Vol. 5. (Ed BJ Miflin) pp. 169–202. (Academic Press: New York)

Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
Oxidative stress, antioxidants and stress tolerance.Crossref | GoogleScholarGoogle Scholar |

Mizutani M, Ohta D (2010) Diversification of P450 genes during land plant evolution. Annual Review of Plant Biology 61, 291–315.
Diversification of P450 genes during land plant evolution.Crossref | GoogleScholarGoogle Scholar |

Mérigout P, Lelandais M, Bitton F, Renou J-P, Briand X, Meyer C, Daniel-Vedele F (2008) Physiological and transcriptomic aspects of urea uptake and assimilation in Arabidopsis plants. Plant Physiology 147, 1225–1238.
Physiological and transcriptomic aspects of urea uptake and assimilation in Arabidopsis plants.Crossref | GoogleScholarGoogle Scholar |

Ng TB, Liu J, Wong JH, Ye X, Wing Sze SC, Tong Y, Zhang KY (2012) Review of research on Dendrobium, a prized folk medicine. Applied Microbiology and Biotechnology 93, 1795–1803.
Review of research on Dendrobium, a prized folk medicine.Crossref | GoogleScholarGoogle Scholar |

Paul MJ, Driscoll SP (1997) Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source:sink imbalance. Plant, Cell & Environment 20, 110–116.
Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source:sink imbalance.Crossref | GoogleScholarGoogle Scholar |

Peng M, Bi Y-M, 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 Molecular Biology 65, 775–797.
Genome-wide analysis of Arabidopsis responsive transcriptome to nitrogen limitation and its regulation by the ubiquitin ligase gene NLA.Crossref | GoogleScholarGoogle Scholar |

Peng M, Hudson D, Schofield A, Tsao R, Yang R, Gu H, Bi Y-M, Rothstein SJ (2008) Adaptation of Arabidopsis to nitrogen limitation involves induction of anthocyanin synthesis which is controlled by the NLA gene. Journal of Experimental Botany 59, 2933–2944.
Adaptation of Arabidopsis to nitrogen limitation involves induction of anthocyanin synthesis which is controlled by the NLA gene.Crossref | GoogleScholarGoogle Scholar |

Perchlik M, Tegeder M (2018) Leaf amino acid supply affects photosynthetic and plant nitrogen use efficiency under nitrogen stress. Plant Physiology 178, 174–188.
Leaf amino acid supply affects photosynthetic and plant nitrogen use efficiency under nitrogen stress.Crossref | GoogleScholarGoogle Scholar |

Pristov JB, Mitrović A, Spasojević I (2011) A comparative study of antioxidative activities of cell-wall polysaccharides. Carbohydrate Research 346, 2255–2259.
A comparative study of antioxidative activities of cell-wall polysaccharides.Crossref | GoogleScholarGoogle Scholar |

Quan X, Zeng J, Ye L, Chen G, Han Z, Shah JM, Zhang G (2016) Transcriptome profiling analysis for two Tibetan wild barley genotypes in responses to low nitrogen. BMC Plant Biology 16, 30
Transcriptome profiling analysis for two Tibetan wild barley genotypes in responses to low nitrogen.Crossref | GoogleScholarGoogle Scholar |

Rao IM, Miles JW, Beebe SE, Horst WJ (2016) Root adaptations to soils with low fertility and aluminium toxicity. Annals of Botany 118, 593–605.
Root adaptations to soils with low fertility and aluminium toxicity.Crossref | GoogleScholarGoogle Scholar |

Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. Journal of Biological Chemistry 279, 11736–11743.
The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Stewart AJ, Bozonnet S, Mullen W, Jenkins GI, Lean MEJ, Crozier A (2000) Occurrence of flavonols in tomatoes and tomato-based products. Journal of Agricultural and Food Chemistry 48, 2663–2669.
Occurrence of flavonols in tomatoes and tomato-based products.Crossref | GoogleScholarGoogle Scholar |

Stewart AJ, Chapman W, Jenkins GI, Graham I, Martin T, Crozier A (2001) The effect of nitrogen and phosphorus deficiency on flavonol accumulation in plant tissues. Plant, Cell & Environment 24, 1189–1197.
The effect of nitrogen and phosphorus deficiency on flavonol accumulation in plant tissues.Crossref | GoogleScholarGoogle Scholar |

Sun Q, Lu H, Zhang Q, Wang D, Chen J, Xiao J, Ding X, Li Q (2021) Transcriptome sequencing of wild soybean revealed gene expression dynamics under low nitrogen stress. Journal of Applied Genetics 62, 389–404.
Transcriptome sequencing of wild soybean revealed gene expression dynamics under low nitrogen stress.Crossref | GoogleScholarGoogle Scholar |

Tang H, Zhao T, Sheng Y, Zheng T, Fu L, Zhang Y (2017) Dendrobium officinale Kimura et Migo: a review on its ethnopharmacology, phytochemistry, pharmacology, and industrialization. Evidence-Based Complementary and Alternative Medicine 2017, 7436259
Dendrobium officinale Kimura et Migo: a review on its ethnopharmacology, phytochemistry, pharmacology, and industrialization.Crossref | GoogleScholarGoogle Scholar |

Tang Y, Wang M, Cao L, Dang Z, Ruan N, Wang Y, Huang Y, Wu J, Zhang M, Xu Z, Chen W, Li F, Xu Q (2022) OsUGE3-mediated cell wall polysaccharides accumulation improves biomass production, mechanical strength, and salt tolerance. Plant, Cell & Environment 45, 2492–2507.
OsUGE3-mediated cell wall polysaccharides accumulation improves biomass production, mechanical strength, and salt tolerance.Crossref | GoogleScholarGoogle Scholar |

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 Phytologist 207, 613–626.
Isoprenoids and phenylpropanoids are part of the antioxidant defense orchestrated daily by drought-stressed Platanus × acerifolia plants during Mediterranean summers.Crossref | GoogleScholarGoogle Scholar |

Tian J, Pang Y, Zhao Z (2021) Drought, salinity, and low nitrogen differentially affect the growth and nitrogen metabolism of Sophora japonica (L.) in a semi-hydroponic phenotyping platform. Frontiers in Plant Science 12, 715456
Drought, salinity, and low nitrogen differentially affect the growth and nitrogen metabolism of Sophora japonica (L.) in a semi-hydroponic phenotyping platform.Crossref | GoogleScholarGoogle Scholar |

Wang R, Guegler K, LaBrie ST, Crawford NM (2000) Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. The Plant Cell 12, 1491–1509.
Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate.Crossref | GoogleScholarGoogle Scholar |

Wang X, Gao J, Zhu Z, Dong X, Wang X, Ren G, Zhou X, Kuai B (2015) TCP transcription factors are critical for the coordinated regulation of ISOCHORISMATE SYNTHASE 1 expression in Arabidopsis thaliana. The Plant Journal 82, 151–162.
TCP transcription factors are critical for the coordinated regulation of ISOCHORISMATE SYNTHASE 1 expression in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Wang F, Wang X, Zhao C, Wang J, Li P, Dou Y, Bi Y (2016) Alternative pathway is involved in the tolerance of highland barley to the low-nitrogen stress by maintaining the cellular redox homeostasis. Plant Cell Reports 35, 317–328.
Alternative pathway is involved in the tolerance of highland barley to the low-nitrogen stress by maintaining the cellular redox homeostasis.Crossref | GoogleScholarGoogle Scholar |

Wang J, Song K, Sun L, Qin Q, Sun Y, Pan J, et al. (2019) Morphological and transcriptome analysis of wheat seedlings response to low nitrogen stress. Plants 8, 98
Morphological and transcriptome analysis of wheat seedlings response to low nitrogen stress.Crossref | GoogleScholarGoogle Scholar |

Wang Y, Tong Y, Adejobi OI, Wang Y, Liu A (2022) Research advances in multi-omics on the traditional chinese herb Dendrobium officinale. Frontiers in Plant Science 12, 808228
Research advances in multi-omics on the traditional chinese herb Dendrobium officinale.Crossref | GoogleScholarGoogle Scholar |

Wei Q, Yan Z, Xiong Y, Fang Z (2021) Altered expression of OsAAP3 influences rice lesion mimic and leaf senescence by regulating arginine transport and nitric oxide pathway. International Journal of Molecular Sciences 22, 2181
Altered expression of OsAAP3 influences rice lesion mimic and leaf senescence by regulating arginine transport and nitric oxide pathway.Crossref | GoogleScholarGoogle Scholar |

Wingler A, Purdy S, MacLean JA, Pourtau N (2006) The role of sugars in integrating environmental signals during the regulation of leaf senescence. Journal of Experimental Botany 57, 391–399.
The role of sugars in integrating environmental signals during the regulation of leaf senescence.Crossref | GoogleScholarGoogle Scholar |

Xin M, Wang L, Liu Y, Feng Z, Zhou X, Qin Z (2017) Transcriptome profiling of cucumber genome expression in response to long-term low nitrogen stress. Acta Physiologiae Plantarum 39, 130
Transcriptome profiling of cucumber genome expression in response to long-term low nitrogen stress.Crossref | GoogleScholarGoogle Scholar |

Xu C, He C (2007) The rice OsLOL2 gene encodes a zinc finger protein involved in rice growth and disease resistance. Molecular Genetics and Genomics 278, 85–94.
The rice OsLOL2 gene encodes a zinc finger protein involved in rice growth and disease resistance.Crossref | GoogleScholarGoogle Scholar |

Yan H, Shi H, Hu C, Luo M, Xu C, Wang S, Li N, Tang W, Zhou Y, Wang C, Xu Z, Chen J, Ma Y, Sun D Yan H, Shi H, Hu C, Luo M, Xu C, Wang S, Li N, Tang W, Zhou Y, Wang C, Xu Z, Chen J, Ma Y, Sun D (2021) Transcriptome Differences in Response Mechanisms to Low-Nitrogen Stress in Two Wheat Varieties. International Journal of Molecular Sciences 22, 12278
Transcriptome Differences in Response Mechanisms to Low-Nitrogen Stress in Two Wheat Varieties.Crossref | GoogleScholarGoogle Scholar |

Yanagisawa S (2000) Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. The Plant Journal 21, 281–288.
Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize.Crossref | GoogleScholarGoogle Scholar |

Yang S, Zhang X, Cao Z, Zhao K, Wang S, Chen M, Hu X (2014) Growth-promoting Sphingomonas paucimobilis ZJSH1 associated with Dendrobium officinale through phytohormone production and nitrogen fixation. Microbial Biotechnology 7, 611–620.
Growth-promoting Sphingomonas paucimobilis ZJSH1 associated with Dendrobium officinale through phytohormone production and nitrogen fixation.Crossref | GoogleScholarGoogle Scholar |

Zakari SA, Zaidi SHR, Sunusi M, Dauda KD (2021) Nitrogen deficiency regulates premature senescence by modulating flag leaf function, ROS homeostasis, and intercellular sugar concentration in rice during grain filling. Journal of Genetic Engineering and Biotechnology 19, 177
Nitrogen deficiency regulates premature senescence by modulating flag leaf function, ROS homeostasis, and intercellular sugar concentration in rice during grain filling.Crossref | GoogleScholarGoogle Scholar |

Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407–409.
An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture.Crossref | GoogleScholarGoogle Scholar |

Zhang J-Y, Cun Z, Wu H-M, Chen J-W (2020) Integrated analysis on biochemical profiling and transcriptome revealed nitrogen-driven difference in accumulation of saponins in a medicinal plant Panax notoginseng. Plant Physiology and Biochemistry 154, 564–580.
Integrated analysis on biochemical profiling and transcriptome revealed nitrogen-driven difference in accumulation of saponins in a medicinal plant Panax notoginseng.Crossref | GoogleScholarGoogle Scholar |

Zhao D, Reddy KR, Kakani VG, Reddy VR (2005) Nitrogen deficiency effects on plant growth, leaf photosynthesis, and hyperspectral reflectance properties of sorghum. European Journal of Agronomy 22, 391–403.
Nitrogen deficiency effects on plant growth, leaf photosynthesis, and hyperspectral reflectance properties of sorghum.Crossref | GoogleScholarGoogle Scholar |

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 and Cell Physiology 56, 455–467.
RNA-Seq-based transcriptome profiling of early nitrogen deficiency response in cucumber seedlings provides new insight into the putative nitrogen regulatory network.Crossref | GoogleScholarGoogle Scholar |

Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247–273.
Salt and drought stress signal transduction in plants.Crossref | GoogleScholarGoogle Scholar |

Zielinski RE (1998) Calmodulin and calmodulin binding proteins in plants. Annual Review of Plant Physiology and Plant Molecular Biology 49, 697–725.
Calmodulin and calmodulin binding proteins in plants.Crossref | GoogleScholarGoogle Scholar |