Beneficial role of acetylcholine in chlorophyll metabolism and photosynthetic gas exchange in Nicotiana benthamiana seedlings under salinity stress.
Acetylcholine
chlorophyll metabolism
gene expression
ion toxicity
root hydraulics
salt stress
Journal
Plant biology (Stuttgart, Germany)
ISSN: 1438-8677
Titre abrégé: Plant Biol (Stuttg)
Pays: England
ID NLM: 101148926
Informations de publication
Date de publication:
May 2020
May 2020
Historique:
received:
01
09
2019
accepted:
18
11
2019
pubmed:
8
12
2019
medline:
19
5
2020
entrez:
8
12
2019
Statut:
ppublish
Résumé
Acetylcholine (ACh) is believed to improve plant growth. However, regulation at biochemical and molecular levels is largely unknown. The present study investigated the impact of exogenously applied ACh (10 µm) on growth and chlorophyll metabolism in hydroponically grown Nicotiana benthamiana under salt stress (150 mm NaCl). Salinity reduced root hydraulic conductivity while ACh-treated seedlings exhibited a significant increase, resulting in increased relative water content. Salinity induced a reduction in chlorophyll biosynthetic intermediates, such as protoporphyrin-IX, Mg-photoporphyrin-IX and protochlorophyllide, which were significantly ameliorated in the presence of ACh. This influence of ACh on chlorophyll synthesis was confirmed by up-regulation of HEMA1, CHLH, CAO and POR genes. Gas exchange parameters, i.e. stomatal conductance, internal CO
Substances chimiques
Chlorophyll
1406-65-1
Acetylcholine
N9YNS0M02X
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
357-365Subventions
Organisme : National Key Research and Development Program of China
ID : 2017YFE0114000
Organisme : Sci-tec Project of China Tobacco Shaanxi Industrial Co. Ltd.
ID : SXYC-2016-KJ-02
Organisme : Sci-tec Project of Shaanxi China Tobacco Industrial Co., Ltd.
ID : JS-FW-2016-001
Informations de copyright
© 2019 German Society for Plant Sciences and The Royal Botanical Society of the Netherlands.
Références
Ahanger M.A., Agarwal R.M. (2017) Salinity stress induced alterations in antioxidant metabolism and nitrogen assimilation in wheat (Triticum aestivum L) as influenced by potassium supplementation. Plant Physiology and Biochemistry, 115, 449-460.
Ahanger M.A., Tyagi S.R., Wani M.R., Ahmad P. (2014) Drought tolerance: roles of organic osmolytes, growth regulators, and mineral nutrients. In: Ahmad P., Wani M. R. (Eds), Physiological mechanisms and adaptation strategies in plants under a changing environment. Springer, Berlin, Germany, pp 25-55.
Ahanger M.A., Agarwal R.M., Tomar N.S., Shrivastava M. (2015) Potassium induces positive changes in nitrogen metabolism and antioxidant system of oat (Avena sativa L cultivar Kent). Journal of Plant Interactions, 10, 211-223.
Ahanger M.A., Tomar N.S., Tittal M., Argal S., Agarwal R.M. (2017) Plant growth under water/salt stress: ROS production, antioxidants and significance of added potassium under such conditions. Physiology and Molecular Biology of Plants, 23, 731-744.
Ahanger M.A., Alyemeni M.N., Wijaya L., Alamri S.A., Alam P., Ashraf M., Ahmad P., Huang Y. (2018) Potential of exogenously sourced kinetin in protecting Solanum lycopersicum from NaCl-induced oxidative stress through up-regulation of the antioxidant system, ascorbate-glutathione cycle and glyoxalase system. PLoS ONE, 13, e0202175.
Akram N.A., Ashraf M. (2013) Regulation in plant stress tolerance by a potential plant growth regulator, 5-aminolevulinic acid. Journal of Plant Growth Regulation, 32, 663-679.
Al-Ghumaiz N.S., Abd-Elmoniem E.M., Motawei M.I. (2017) Salt tolerance and K/Na ratio of some introduced forage grass species under salinity stress in irrigated areas. Communications in Soil Science and Plant Analysis, 48, 1494-1502.
Almeida D.M., Oliveira M.M., Saibo N.J.M. (2017) Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants. Genetics and Molecular Biology, 40, 326-345.
Ashraf M. (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnology Advances, 27, 84-93.
Assaha D.V.M., Ueda A., Saneoka H., Al-yahyai R., Yaish M.W. (2017) The role of Na+ and K+ transporters in salt stress adaptation in Glycophytes. Frontiers in Physiology, 8, 509.
Braga I., Pissolato M.D., Souza G.M. (2017) Mitigating effects of acetylcholine supply on soybean seed germination under osmotic stress. Brazilian Journal of Botany, 40, 617-624.
Catinot J., Buchala A., Abou-Mansour E., Métraux J.P. (2008) Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana. FEBS Letters, 582, 473-478.
Chen J., Zhang H.Q., Zhang X.L., Tang M. (2017) Arbuscular mycorrhizal symbiosis alleviates salt stress in black locust through improved photosynthesis, water status, and K+/Na+ homeostasis. Frontiers in Plant Science, 8, 1739.
Dalal V.K., Tripathy B.C. (2012) Modulation of chlorophyll biosynthesis by water stress in rice seedlings during chloroplast biogenesis. Plant, Cell and Environment, 35, 1685-1703.
Deng B.L., Jin X.H., Yang Y., Lin Z.W., Zhang Y.L. (2014) The regulatory role of riboflavin in the drought tolerance of tobacco plants depends on ROS production. Plant Growth Regulation, 72, 269-277.
Deng X.G., Zhu T., Zhang D.W., Lin H.H. (2015) The alternative respiratory pathway is involved in brassinosteroid-induced environmental stress tolerance in Nicotiana benthamiana. Journal of Experimental Botany, 66, 6219-6232.
Feller U., Kingston-Smith A.H., Centritto M. (2017) Abiotic stresses in agroecology: a challenge for whole plant physiology. Frontiers in Environmental Science, 5, 13.
Gao J.F. (2006) Plant physiology experiment instruction. Science Press, Beijing, China.
Hasegawa P.M. (2013) Sodium (Na+) homeostasis and salt tolerance of plants. Environmental and Experiment Botany, 92, 19-31.
Hauser F., Horie T. (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant, Cell and Environment, 33, 552-565.
Hayat S., Yadav S., Wani A.S., Irfan M., Alyemini M.N., Ahmad A. (2012) Impact of sodium nitroprusside on nitrate reductase, proline content, and antioxidant system in tomato under salinity stress. Horticulture, Environment and Biotechnology, 53, 362-367.
Hodgins R.R., Huystee R.B.V. (1986) Rapid simultaneous estimation of protoporphyrin and Mg-porphyrins in higher plants. Journal of Plant Physiology, 125, 311-323.
Hu L., Xiang L., Li S., Zou Z., Hu X. (2015) Beneficial role of spermidine in chlorophyll metabolism and D1 protein content in tomato seedlings under salinity-alkalinity stress. Physiologia Plantarum, 156, 468-477.
Kawashima K., Misawa H., Moriwaki Y., Fujii Y.X., Fujii T., Horiuchi Y., Yamada T., Imanaka T., Kamekura M. (2007) Ubiquitous expression of acetylcholine and its biological functions in life forms without nervous systems. Life Science, 80, 2206-2209.
Khan M.N., Siddiqui M.H., Mohammad F., Naeem M. (2012) Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide, 27, 210-218.
Krishna T.S., Madhusmita P., Saivishnupriya K., Nirosha P., Sarla N., Rajeshwari R. (2016) Cytokinin delays dark-induced senescence in rice by maintaining the chlorophyll cycle and photosynthetic complexes. Journal of Experimental Botany, 67, 1839-1851.
Lichtenthaler H.K. (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350-382.
Liu P., Yin L.N., Deng X.P., Wang S.W., Tanaka K., Zhang S.Q. (2014) Aquaporin-mediated increase in root hydraulic conductance is involved in silicon-induced improved root water uptake under osmotic stress in Sorghum bicolor L. Journal of Experimental Botany, 65, 4747-4756.
Ma L.J., Li Y.Y., Yu C.M., Wang Y., Li X.M., Li N., Chen Q., Bu N. (2012) Alleviation of exogenous oligochitosan on wheat seedlings growth under salt stress. Protoplasma, 249, 393-399.
Mittler R., Vanderauwera S., Gollery M., Van B.F. (2004) Reactive oxygen gene network of plants. Trends in Plant Science, 9, 490-498.
Moradi F., Ismail A.M. (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Annals of Botany, 99, 1161-1173.
Munns R., Tester M. (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology, 59, 651-681.
Nagahatenna D.S.K., Langridge P., Whitford R. (2015) Tetrapyrrole-based drought stress signaling. Plant Biotechnology Journal, 13, 447-459.
Oukarroum A., Bussotti F., Goltsev V., Kalaji H.M. (2015) Correlation between reactive oxygen species production and photochemistry of photosystems I and II in Lemna gibba L. plants under salt stress. Environmental and Experimental Botany, 109, 80-88.
Papenbrock J., Pfündel E., Mock H.P., Grimm B. (2000) Decreased and increased expression of the subunit CHL I diminishes Mg chelatase activity and reduces chlorophyll synthesis in transgenic tobacco plants. The Plant Journal, 22, 155-164.
Pfaffl M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, e45.
Phung T.H., Jung H.I., Park J.H., Kim J.G., Back K., Jung S. (2011) Porphyrin biosynthesis control under water stress: sustained porphyrin status correlates with drought tolerance in transgenic rice. Plant Physiology, 157, 1746-1764.
Qin C., Su Y.Y., Li B.S., Cheng Y.Q., Wei C.C., Yuan S., Ahmed N., Ashraf M., Zhang L.X. (2019) Acetylcholine mechanism of action to enhance tolerance to salt stress in Nicotiana benthamiana. Photosynthetica, 57, 590-598.
Rasheed R., Wahid A., Hussain I., Mahmood S., Parveen A. (2016) Partial repair of salinity-induced damage to sprouting sugarcane buds by proline and glycinebetaine pretreatment. Protoplasma, 253, 803-813.
Roshchina V.V., Roshchina V.V. (2001) Neurotransmitters in plant life. Phytochemistry, 63, 373-374.
Rossi S., Burgess P., Jespersen D., Huang B. (2017) Heat-induced leaf senescence associated with chlorophyll metabolism in Bentgrass lines differing in heat tolerance. Crop Science, 57, 169-178.
Roy S.J., Negrao S., Tester M. (2014) Salt resistant crop plants. Current Opinion in Biotechnology, 26, 115-124.
Ruizlozano J.M., Porcel R., Azcón C., Aroca R. (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. Journal of Experimental Botany, 63, 4033-4044.
Rus A., Lee B.H., Munoz-Mayor A., Sharkhuu A., Miura K., Zhu J.K., Bressan R.A., Hasegawa P.M. (2004) AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiology, 136, 2500-2511.
Sagane Y., Nakagawa T., Yamamoto K., Michikawa S., Oguri S., Momonoki Y.S. (2005) Molecular characterization of maize acetylcholinesterase: a novel enzyme family in the plant kingdom. Plant Physiology, 138, 1359-1371.
Sansebastiano G.P.D., Fornaciari S., Barozzi F., Piro G., Arru L. (2014) New insights on plant cell elongation: a role for acetylcholine. International Journal of Molecular Sciences, 15, 4565-4582.
Tanaka A., Tanaka R. (2006) Chlorophyll metabolism. Current Opinion in Biotechnology, 9, 248-255.
Tretyn A., Kendrick R.E. (1991) Acetylcholine in plants: presence, metabolism and mechanism of action. Botanical Review, 57, 33-73.
Trubat R., Corona J., Vilagrosa A. (2012) Root architecture and hydraulic conductance in nutrient deprived Pistacia lentiscus L. seedlings. Oecologia, 170, 899-908.
Turan S., Tripathy B.C. (2015) Salt-stress induced modulation of chlorophyll biosynthesis during de-etiolation of rice seedlings. Physiologia Plantarum, 153, 477-491.
Wang H.B., Zhang S.Q., Wang X.C., Lou C.H. (2003) Involvement of Ca2+/CaM in the signal transduction of acetylcholine regulating stomatal movement. Chinese Science Bulletin, 48, 351-354.
Wang Y., Weide R., Govers F., Bouwmeester K. (2015) L-type lectin receptor kinases in Nicotiana benthamiana and tomato and their role in Phytophthora resistance. Journal of Experimental Botany, 66, 6731-6743.
Wessler L., Kilbinger H., Bittinger F., Kirkpatrick C.J. (2001) The biological role of non-neuronal acetylcholine in plants and humans. Japanese Journal of Pharmacology, 85, 2-10.
Wu Y., Jin X., Liao W., Hu L., Dawuda M.M., Zhao X., Yu J. (2018) 5-Aminolevulinic acid (ALA) alleviated salinity stress in cucumber seedlings by enhancing chlorophyll synthesis pathway. Frontiers in Plant Science, 9, 635.
Xi Z.M., Wang Z.Z., Fang Y.L., Hu Z.Y., Hu Y., Deng M.M., Zhang Z.W. (2013) Effects of 24-epibrassinolide on antioxidation defense and osmoregulation systems of young grapevines (V. vinifera L.) under chilling stress. Plant Growth Regulation, 71, 57-65.
Yamamoto K., Oguri S., Momonoki Y.S. (2008) Characterization of trimeric acetylcholinesterase from a legume plant, Macroptilium atropurpureum Urb. Planta, 227, 809-822.
Yamamoto K., Oguri S., Chiba S., Momonoki Y.S. (2009) Molecular cloning of acetylcholinesterase gene from Salicornia europaea L. Plant Signaling & Behavior, 4, 361-366.
Yuan R.N., Shu S., Guo S.R., Sun J., Wu J.Q. (2018) The positive roles of exogenous putrescine on chlorophyll metabolism and xanthophyll cycle in salt-stressed cucumber seedlings. Photosynthetica, 56, 557-566.
Zhang J., Duan X.H., Ding F., Ma H.Z., Zhang T.G., Yang Y.L. (2014) Salinity induced the changes of root growth and antioxidative responses in two wheat cultivars. Protoplasma, 251, 771-780.
Zhu J.K. (2003) Regulation of ion homeostasis under salt stress. Current Opinion in Plant Biology, 6, 441-445.