园艺-栽培生理/资源品质合辑Horticulture — Physiology · Biochemistry · Cultivation
|The mitigation effects of exogenous dopamine on low nitrogen stress in Malus hupehensis
|LIU Xiao-min, GAO Teng-teng, ZHANG Zhi-jun, TAN Ke-xin, JIN Yi-bo, ZHAO Yong-juan, MA Feng-wang, LI Chao
|State Key Laboratory of Crop Stress Biology for Arid Areas, Ministry of Science and Technology/Shaanxi Key Laboratory of Apple, Northwest A&F University, Yangling 712100, P.R.China
Dopamine plays numerous physiological roles in plants. We explored its role in the regulation of growth, nutrient absorption, and response to nitrogen (N) deficiency in Malus hupehensis Rehd. Under low N condition, plant growth slowed, and the net photosynthetic rates, chlorophyll contents, and maximal quantum yield of PSII (Fv/Fm) decreased significantly. However, the application of 100 μmol L−1 exogenous dopamine significantly reduced the inhibition of low N stress on plant growth. In addition to modifying root system architecture under low N supply, exogenous dopamine also changed the uptake, transport, and distribution of N, P, and K. Furthermore, exogenous dopamine enhances the tolerance to low nitrogen stress by increasing the activity of enzymes (nitrate reductase, nitrite reductase, glutamic acid synthase and glutamine synthetase) involved in N metabolism. We also found that exogenous dopamine promoted the expression of ethylene signaling genes (ERF1, ERF2, EIL1, ERS2, ETR1, and EIN4) under low N stress. Therefore, we hypothesized that ethylene might be involved in dopamine response to low N stress in M. hupehensis. Our results suggest that exogenous dopamine can mitigate low N stress by regulating the absorption of mineral nutrients, possibly through the regulation of the ethylene signaling pathway.
Received: 18 February 2020
|Fund: This work was supported by the National Key Research and Development Program of China (2018YFD1000303), the National Natural Science Foundation of China (31972389), the Natural Science Basic Research Plan in Shaanxi Province, China (2018JQ3001) and Cyrus Tang Foundation, Northwest A&F University, China.
Correspondence LI Chao, Tel/Fax: +86-29-87082648, E-mail: email@example.com
|About author: LIU Xiao-min, E-mail: firstname.lastname@example.org;
Cite this article:
LIU Xiao-min, GAO Teng-teng, ZHANG Zhi-jun, TAN ke-xin, JIN Yi-bo, ZHAO Yong-juan, MA Feng-wang, LI Chao.
The mitigation effects of exogenous dopamine on low nitrogen stress in Malus hupehensis. Journal of Integrative Agriculture, 19(11): 2709-2724.
| Antal T, Mattila H, Hakala-Yatkin M, Tyystjarvi T, Tyystjarvi E. 2010. Acclimation of photosynthesis to nitrogen deficiency in Phaseolus vulgaris. Planta, 232, 887–898.
Arnon D I. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiololy, 24, 1.
Baker N R. 2008. Chlorophyll fluorescence, a probe of photosynthesis in vivo. Annual Review of Plant Biology, 59, 89–113.
Boussadia O, Steppe K, Zgallai H, Hadj S B E, Braham M, Lemeur R, Labeke M C V. 2010. Effects of nitrogen deficiency on leaf photosynthesis, carbohydrate status and biomass production in two olive cultivars ‘Meski’ and ‘Koroneiki’. Scientia Horticulturae, 123, 336–342.
Britto D T, Kronzucker H J. 2006. Plant nitrogen transport and its regulation in changing soil environments. Journal of Crop Improvement, 15, 1–23.
Caputo C, Criado M V, Roberts I N, Gelso M A, Barneix A J. 2009. Regulation of glutamine synthetase 1 and amino acids transport in the phloem of young wheat plants. Plant Physiology and Biochemistry, 47, 335–342.
Chen C L. 2003. Measurement of plant root activity (TTC). In: Li H S, ed., Principle and Technology of Plant Physiological and Biochemical Experiments. Higher Education Press, Beijing. (in Chinese)
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.
Ciompi S, Gentili E, Guidi L, Soldatini G F. 1996. The effect of nitrogen deficiency on leaf gas exchange and chlorophyll fluorescence parameters in sunflower. Plant Science, 118, 177–184.
Dai Y R, Michaels P J, Flores H E. 1993. Stimulation of ethylene production by catecholamines and phenylethylamine in potato cell suspension cultures. Plant Growth Regulation, 12, 219–222.
D’Hooghe P, Escamez S, Trouverie J, Avice J C. 2013. Sulphur limitation provokes physiological and leaf proteome changes in oilseed rape that lead to perturbation of sulphur, carbon and oxidative metabolisms. BMC Plant Biology, 13, 23.
Dionisio-Sese M L, Tobita S. 1998. Antioxidant responses of rice seedings to salinity stress. Plant Science, 135, 1–9.
Elstner E F, Konze J R, Selman B R, Stoffer C. 1976. Ethylene formation in sugar beet leaves: evidence for the involvement of 3-hydroxytyramine and phenoloxidase after wounding. Plant Physiology, 58, 163–168.
Facchini P J, Yu M, Penzesyost C. 1999. Decreased cell wall digestibility in canola transformed with chimeric tyrosine decarboxylase genes from opium poppy. Plant Physiololy, 120, 653–663.
Feng F, Zhang F S, Yang X Q. Research on Plant Nutrition: Progress and Prospect. 2000. China Agricultural University Press, Beijing. (in Chinese)
Fuchs Y. 1970. Ethylene production by citrus fruit peel: Stimulation by phenol derivatives. Plant Physiology, 45, 533–534.
Gao T T, Zhang Z J, Liu X M, Wu Q, Chen Q, Liu Q W, van Nocker S, Ma F W, Li C. 2020. Physiological and transcriptome analyses of the effects of exogenous dopamine on drought tolerance in apple. Plant Physiology and Biochemistry, 148, 260–272.
García M J, Romera F J, Lucena C, Alcántara E, Pérez-Vicente R. 2015. Ethylene and the regulation of physiological and morphological responses to nutrient deficiencies. Plant Physiology, 169, 51–60.
Glasbey C A, Hunt R. 1983. Plant growth curves: The functional approach to plant growth analysis. Biometrics, 39, 537.
Gruber B D, Giehl R F H, Friedel S, Wirén N. 2013. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology, 163, 161–179.
He C J, Morgan P W, Drew M C. 1992. Enhanced sensitivity to ethylene in nitrogen- or phosphate-starved roots of Zea mays L. during aerenchyma formation. Plant Physiology, 98, 137–142.
Hermans C, Hammond J P, White P J, Verbruggen N. 2006. How do plants respond to nutrient shortage by biomass allocation? Plant Science, 11, 610–617.
Hermans C, Vuylsteke M, Coppens F, Cristescu S M, Harren F J M, Inzé D, Verbruggen N. 2010. Systems analysis of the responses to long-term magnesium deficiency and restoration in Arabidopsis thaliana. New Phytologist, 187, 132–144.
Hirel B, Bertin P, Quillere I, Bourdoncle W, Attagnant C, Dellay C, Gouy A, Cadiou S, Retailliau C, Falque M, Gallais A. 2001. Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiology, 125, 1258–1270.
Hodge A. 2004. Hormone interactions during lateral root formation. New Phytologist, 162, 9–24.
Huang D, Ma M N, Wang Q, Zhang M X, Jing G Q, Li C, Ma F W. 2020. Arbuscular mycorrhizal fungi enhanced drought resistance in apple by regulating genes in the MAPK pathway. Plant Physiology and Biochemistry, 149, 245–255.
Huo L Q, Sun X, Guo Z J, Jia X, Che R M, Sun Y M, Zhu Y F, Wang P, Gong X Q, Ma F W. 2020. MdATG18a overexpression improves basal thermotolerance in transgenic apple by decreasing damage to chloroplasts. Horticulture Research, 7, 21.
Ivanchenko M G, Muday G K, Dubrovsky J G. 2008. Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. The Plant Journal, 55, 335–347.
Jung J Y, Shin R, Schachtman D P. 2009. Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis. The Plant Cell, 21, 607–621.
Kanazawa K, Sakakibara H. 2000. High content of dopamine, a strong antioxidant, in Cavendish banana. Food Chemistry, 48, 844–848.
Kim M J, Ruzicka D, Shin R, Schachtman D P. 2012. The Arabidopsis AP2/ERF transcription factor RAP2.11 modulates plant response to low-potassium conditions. Molecular Plant, 5, 1042–1057.
Kolber Z, Falkowski Z P. 1988. Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in photosystem II. Plant Physiology, 88, 923–929.
Kraiser T, Gras E, Gutierrez A G, Gonzalez, B, Gutierrez R A. 2011. A holistic view of nitrogen acquisition in plants. Journal of Experimental Botany, 62, 1455–1466.
Krapp A. 2015. Plant nitrogen assimilation and its regulation: A complex puzzle with missing pieces. Current Opinion in Plant Biology, 25, 115–122.
Kruse J, Kopriva S, Haensch R, Krauss G J, Mendel R R, Rennenberg H. 2007. Interaction of sulfur and nitrogen nutrition in tobacco (Nicotiana tabacum) plants: Significance of nitrogen source and root nitrate reductase. Plant Biology, 9, 638–646.
Kuklin A I, Conger B V. 1995. Catecholamines in plants. Journal of Plant Growth Regulation, 14, 91–97.
Kulma A, Szopa J. 2007. Catecholamines are active compounds in plants. Plant Science, 172, 433–440.
Leblanc A, Renault H, Lecourt J, Etienne P, Deleu C, Le Deunff E. 2008. Elongation changes of exploratory and root hair systems induced by aminocyclopropane carboxylic acid and aminoethoxyvinylglycine affect nitrate uptake and BnNrt2.1 and BnNrt1.1 transporter gene expression in oilseed rape. Plant Physiology, 146, 1928–1940.
Lei M, Zhu C, Liu Y, Karthikeyan A S, Bressan R A, Raghothama K G, Liu D. 2011. Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. New Phytologist, 189, 1084–1095.
Li C, Liang B W, Chang C, Wei Z W, Zhou S S, Ma F W. 2016. Exogenous melatonin improved potassium content in Malus under different stress conditions. Journal of Pineal Research, 61, 218–229.
Li C, Sun X K, Chang C, Jia D F, Wei Z W, Li C, Ma F W. 2015. Dopamine alleviates salt-induced stress in Malus hupehensis. Physiologia Plantarum, 153, 584–602.
Li S W, Wen H, Zhou Y Z, Li Y M, Xiao K. 2006. Characterization of nitrogen uptake and dry matter production in wheat varieties with different N efficiency. Scientia Agricultura Sinica, 39, 1999–2000. (in Chinese)
Liang B, Li C Y, Ma C Q, Wei Z W, Wang Q, Huang D, Chen Q, Li C, Ma F W. 2017. Dopamine alleviates nutrient deficiency-induced stress in Malus hupehensis. Plant Physiology and Biochemistry, 119, 346–359.
Liao H, Yan X L. 2003. Advanced Plant Nutrition. Science Press, Beijing. (in Chinese)
Liu D P, Li M X, Liu Y, Shi L X. 2020. Integration of the metabolome and transcriptome reveals the resistance mechanism to low nitrogen in wild soybean seedling roots. Environmental and Experimental Botany, 175, doi: 10.1016/j.envexpbot.2020.104043
Lu C, Zhang J, Zhang Q, Li L, Kuang T. 2001. Modification of photosystem II photochemistry in nitrogen deficient maize and wheat plants. Journal of Plant Physiology, 158, 1423–1430.
Luo J, Li H, Liu T X, Polle A, Peng C H, Luo Z B. 2013. Nitrogen metabolism of two contrasting poplar species during acclimation to limiting nitrogen availability. Journal of Experimental Botany, 64, 4207–4224.
Ma Y Y, Gai Y, Chen W Q, Jiang X N. 2008. Quantitative determination of 1-aminocyclopropane-1-carboxylic acid (ACC) content in trace of plant tissues by high performance liquid chromatography-electrospray tandem mass spectrometry (HPLC-ESI/MSn). Plant Physiology Communications, 4, 754–758. (in Chinese)
Mahmoud D, Pandey R, Sathee L, Dalal M, Singh M P, Chinnusamy V. Regulation of expression of genes associated with nitrate response by osmotic stress and combined osmotic and nitrogen deficiency stress in bread wheat (Triticum aestivum L.). Plant Physiology Reports, 25, 200–215.
Marschner H. 1995. Mineral Nutrition of Higher Plants. Academic Press, London. pp. 229–312.
Martin T, Oswald O, Graham I A. 2002. Arabidopsis seedling growth, storage lipid mobilization, and photosynthetic gene expression are regulated by carbon: Nitrogen availability. Plant Physiology, 128, 472–481.
Martín-Rejano E M, Camacho-Cristóbal J J, Herrera-Rodríguez M B, Rexach J, Navarro-Gochicoa M T, González-Fontes A. 2011. Auxin and ethylene are involved in the responses of root system architecture to low boron supply in Arabidopsis seedlings. Physiology Plant, 142, 170–178.
Moniuszko G, Skoneczny M, Zientara-Rytter K, Wawrzynska A, Glow D, Cristescu S M, Harren F J M, Sirko A. 2013. Tobacco LSU-like protein couples sulphur-deficiency response with ethylene signalling pathway. Journal of Experimental Botany, 64, 5173–5182.
Protacio C M, Dai Y R, Lewis E F, Flores H E. 1992. Growth stimulation by catecholamines in plant tissue/organ cultures. Plant Physiology, 98, 89–96.
Radford P J. 1967. Growth analysis formulae - their use and abuse. Crop Science, 7, 171–175.
Rao I M, Miles J W, Beebe S E, Horst W J. 2016. Root adaptations to soils with low fertility and aluminium toxicity. Annals of Botany, 118, 593–605.
Romera F J, Alcantara E, Guardia M D D L. 1999. Ethylene production by Fe-deficient roots and its involvement in the regulation of Fe-deficiency stress responses by strategy I plants. Annals of Botany, 83, 51–55.
Roshchina V V. 1990. Biomediators in chloroplasts of higher plants. 3. Effect of dopamine on photochemical activity. Photosynthetica, 24, 117–121.
Rubio V, Bustos R, Irigoyen M L, Cardona-López X, Rojas-Triana M, Paz-Ares J. 2009. Plant hormones and nutrient signaling. Plant Molecular Biology, 69, 361–373.
Schmelz E A, Alborn H T, Engelberth J, Tumlinson J H. 2003. Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize. Plant Physiology, 133, 295–306.
Schmidt W, Schikora A. 2001. Different pathways are involved in phosphate and iron stress-induced alterations of root epidermal cell development. Plant Physiology, 125, 2078–2084.
Suzuki M, Mizoguchi M, Yano F, Hara U, Yokoyama M, Watanabe N. 2003. Changes in catecholamine levels in short day-induced cotyledons of Pharbitis nil. Zeitschrift für Naturforschung C, 58, 3–4.
Tantray A Y, Bashir S S, Ahmad A. 2020. Low nitrogen stress regulates chlorophyll fluorescence in coordination with photosynthesis and Rubisco efficiency of rice. Physiology and Molecular Biology of Plants, 26, 83–94.
Terao T, Katoh S. 1996. Antenna sizes of photosystem I and photosystem II in chlorophyll b-deficient mutants of rice. Evidence for an antenna function of photosystem II centers that are inactive in electron transport. Plant and Cell Physiology, 37, 307–312.
Xu C P, Jiang Z C, Huang B R. 2011. Nitrogen deficiency-induced protein changes in immature and mature leaves of creeping bentgrass. Journal of the American Society for Horticultural Science, 136, 399–407.
Zhan A, Lynch J P. 2015. Reduced frequency of lateral root branching improves N capture from low-N soils in maize. Journal of Experimental Botany, 66, 2055–2065.
Zhang D Y, Zhang Y Q, Yang W D, Miao G Y. 2006. Biological response of roots in different spring wheat genotypes to low nitrogen stress. Acta Agronomica Sinica, 32, 1349–1354. (in Chinese)
Zhang H, Forde B G. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science, 279, 407–409.
Zhao M, Liu W, Xia X, Wang T, Zhang W H. 2014. Cold acclimation-induced freezing tolerance of Medicago truncatula seedlings is negatively regulated by ethylene. Physiologia Plantarum, 152, 115.
|No Suggested Reading articles found!