丛枝菌根通过调节碳磷代谢相关基因的表达增强植物对低磷胁迫的适应性
网络出版日期: 2017-09-29
基金资助
中国科学院战略性先导科技专项(XDB15030102)
Arbuscular mycorrhiza improves plant adaptation to phosphorus deficiency through regulating the expression of genes relevant to carbon and phosphorus metabolism
Online published: 2017-09-29
丛枝菌根(AM)共生体系对于植物适应低磷胁迫具有重要作用。AM不仅直接调节宿主植物对低磷胁迫的响应, 还可能通过分泌物影响相邻的非菌根植物。该研究采用分室培养系统, 以玉米(Zea mays)和AM真菌Rhizophagus irregularis为试验材料, 考察低磷(10 mg·kg-1)和高磷(100 mg·kg-1)条件下, 菌根共生体系对植物生长、磷营养以及碳磷代谢相关基因表达的影响, 以揭示AM调节植物低磷胁迫响应的生理机制。分室培养系统由0.45 μm微孔滤膜分隔成供体室、缓冲室和受体室3个分室, 以供体室菌根化植物为AM分泌物来源, 通过微孔膜阻止菌根真菌对未接种受体植物的直接影响, 但允许AM分泌物在分室间的扩散。采用实时荧光定量PCR技术分析玉米以及AM真菌自身碳磷代谢相关基因的表达情况。试验结果表明, 低磷条件下接种AM真菌显著提高了供体植物干质量和磷浓度, 上调了玉米碳磷代谢相关基因的表达。AM真菌磷转运蛋白基因和碳代谢相关基因在低磷条件下的表达水平显著高于高磷水平; 对于受体植物而言, 仅高磷处理显著提高了玉米植株干质量和磷含量, 而接种处理显著上调了受体植物磷转运蛋白基因和碳代谢相关基因的表达水平。该研究表明, 低磷胁迫下AM可能通过分泌物调控植物碳磷代谢相关基因的表达, 进而调节植物对低磷胁迫的生理响应。
徐丽娇, 姜雪莲, 郝志鹏, 李涛, 吴照祥, 陈保冬 . 丛枝菌根通过调节碳磷代谢相关基因的表达增强植物对低磷胁迫的适应性[J]. 植物生态学报, 2017 , 41(8) : 815 -825 . DOI: 10.17521/cjpe.2017.0018
Aims Arbuscular mycorrhizal (AM) symbiosis plays an important role in plant adaptation to phosphorus (P) deficiency. The mycorrhizal fungi can directly regulate P stress response of the host plants, and can also indirectly influence neighbor plants via AM exudates. This study aimed to reveal the regulation mechanisms of plant response to P deficiency by AM associations. Methods In a compartmentation cultivation experiment with Zea mays ‘B73’ and AM fungus Rhizophagus irregularis ‘DAOM197198’, we investigated mycorrhizal effects on plant P nutrition and the expression of plant and fungal genes related to P and carbon (C) metabolisms under both low P (10 mg?kg-1) and high P (100 mg?kg-1) conditions. The cultivation system consisted of three compartments, namely donor compartment, buffer compartment and receiver compartment divided by two pieces of microporous filters with pore size of 0.45 μm. Maize plant in donor compartment inoculated with AM fungus served as a source of AM exudates. The microporous filters could restrict the development of extraradical mycelium of AM fungi, but allow diffusion of AM exudates. Real-time PCR was performed to quantify the gene expression levels both in maize plants and AM fungi. Important findings The experimental results indicated that under low P conditions mycorrhizal colonization increased plant dry weight and P concentration in donor plants, and up-regulated plant genes encoding P transporters Pht1;2, Pht1;6, phosphoenolpiruvate carboxylase (PEPC), inorganic pyrophosphatase (TC289), glycerol-3-phosphate transporter (G3PT) and malate synthase (MAS1). The expression of AM fungal genes encoding P transporter (GiPT), GlcNAc transporter (NGT1), GlcNAc kinase (HXK1b), GlcNAc phosphomutase (AGM1), UDP GlcNAc pyrophosphorylase (UAP1), chitin synthase (CHS1), GlcNAc-6-phosphate deacetylase (DAC1) and glucosamine-6-phosphate isomerase (NAG1) was significantly higher under low P conditions compared with high P conditions. However, for the receiver plants, plant dry mass and P concentration were only significantly increased by higher P addition, while inoculation treatment significantly up-regulated the expression of P transporter genes Pht1;2 and Pht1;6, C metabolism related genes G3PT, PEPC, TC289 and MAS1. The study proved that AM exudates could potentially stimulate plant response to P deficiency by regulating functional genes relevant to P and C metabolisms in the mycorrhizal associations.
[1] | Bago B, Pfeffer PE, Shachar-Hill Y (2000). Carbon metabolism and transport in arbuscular mycorrhizas.Plant Physiology, 124, 949-958. |
[2] | Bao SD (2000). Soil and Agricultural Chemistry Analysis. China Agriculture Press, Beijing. 81.(in Chinese)[鲍士旦 (2000). 土壤农化分析. 中国农业出版社, 北京. 81.] |
[3] | Barto EK, Hilker M, Müller F, Mohney BK, Weidenhamer JD, Rillig MC (2011). The fungal fast lane: Common mycorrhizal networks extend bioactive zones of allelochemicals in soils.PLOS ONE, 6, e27195. doi: 10.1371/ journal.pone.0027195. |
[4] | Biermann B, Linderman RG (1981). Quantifying vesicular- arbuscular mycorrhizae: A proposed method towards standardization.New Phytologist, 87, 63-67. |
[5] | Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini C, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhardt D (2010). Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning.The Plant Journal, 64, 1002-1017. |
[6] | Carlos CV, Enrique IL, Juan CP, Herrera-Estrella L (2008). Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant-and species- specific levels.Journal of Experimental Botany, 59, 2479-2497. |
[7] | Casieri L, Lahmidi NA, Doidy J, Veneault-Fourrey C, Migeon A, Bonneau L, Courty P, Garcia K, Charbonnier M, Delteil A, Brun A, Zimmermann S, Plassard C, Wipf D (2013). Biotrophic transportome in mutualistic plant-fungal interactions.Mycorrhiza, 23, 597-625. |
[8] | Chabaud M, Genre A, Sieberer BJ, Faccio A, Fournier J, Novero M, Barker DG, Bonfante P (2011). Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis.New Phytologist, 189, 347-355. |
[9] | Chen A, Hu J, Sun S, Xu G (2007). Conservation and divergence of both phosphate- and mycorrhiza-regulated physiological responses and expression patterns of phosphate transporters in solanaceous species.New Phytologist, 173, 817-831. |
[10] | Cunningham JE, Kuiack C (1992). Production of citric and oxalic acids and solubilization of calcium phosphate by Penicillium bilaii.Applied and Environmental Microbiology, 58, 1451-1458. |
[11] | Fixen P (2002). Soil test levels in North America.Better Crops, 86, 12-15. |
[12] | Fukayama H, Hatch MD, Tamai T, Tsuchida H, Sudoh S, Furbank RT, Miyao M (2003). Activity regulation and physiological impacts of maize C4-specific phosphoenolpyruvate carboxylase overproduced in transgenic rice plants.Photosynthesis Research, 77, 227-239. |
[13] | Gardner WK, Barber DA, Parbery DG (1983). The acquisition of phosphorus by Lupinus albus L.: 3. The probable mechanism by which phosphorus movement in the soil/ root interface is enhanced.Plant Soil, 70, 107-124. |
[14] | Gu M, Chen AQ, Dai XL, Liu W, Xu G (2011). How does phosphate status influence the development of the arbuscular mycorrhizal symbiosis?Plant Signalling and Behavior, 6, 1300-1304. |
[15] | Guimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U (2005). Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization.Proceedings of the National Academy of Sciences of the United States of America, 102, 8066-8070. |
[16] | Gutjahr C, Casieri L, Paszkowski U (2009). Glomus intraradices induces changes in root system architecture of rice independently of common symbiosis signaling.New Phytologist, 182, 829-837. |
[17] | Harrison MJ, Dewbre GR, Liu J (2002). A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi.Plant Cell, 14, 2413-2429. |
[18] | Harrison MJ, Pumplin N, Breuillin FJ, Noar RD, Park HJ (2010). Phosphate transporters in arbuscular mycorrhizal symbiosis. In: Koltai H, Kapulnik Y eds. Arbuscular Mycorrhizas: Physiology and Function. Springer, Dordrecht, The Netherlands. 117-135. |
[19] | Javot H, Pumplin N, Harrison M (2007). Phosphate in the arbuscular mycorrhizal symbiosis: Transport properties and regulatory roles.Plant, Cell & Environment, 30, 310-322. |
[20] | Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarié J, Barker DG, Bécard G (2003). A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula.Plant Physiology, 131, 952-962. |
[21] | Li T, Chen BD (2012). Arbuscular mycorrhizal fungi improving drought tolerance of maize plants by up-regulation of aquaporin gene expressions in roots and the fungi themselves.Chinese Journal of Plant Ecology, 36, 973-981.(in Chinese with English abstract)[李涛, 陈保冬 (2012). 丛枝菌根真菌通过上调根系及自身水孔蛋白基因表达提高玉米抗旱性, 植物生态学报,36, 973-981.] |
[22] | Maillet F, Poinsot V, Andre O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Bécard G, Dénarié J (2011). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza.Nature, 469, 58-63. |
[23] | Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001). A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment.Molecular Plant-Microbe Interactions, 14, 1140-1148. |
[24] | Marschner H (1995).Mineral Nutrition of Higher Plants. 2nd edn. Academic Pres. London. |
[25] | Nagy F, Karandashov V, Chague W, Kalinkevich K, Tamasloukht MB, Xu G, Jakobsen I, Levy AA, Amrhein N, Bucher M (2005). The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species.The Plant Journal, 42, 236-250. |
[26] | Nagy R, Drissner D, Amrhein N, Jakobsen I, Bucher M (2009). Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated.New Phytologist, 181, 950-959. |
[27] | Oláh B, Brière C, Bécard G, Dénarié J, Gough C (2005). Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway.The Plant Journal, 44, 195-207. |
[28] | Olsson PA, Hansson MC, Burleigh SH (2006). Effect of P availability on temporal dynamics of carbon allocation and Glomus intraradices high-affinity P transporter gene induction in arbuscular mycorrhiza.Applied and Environmental Microbiology, 72, 4115-4120. |
[29] | Pfaffl MW (2001). A new mathematical model for relative quantification in real-time RT-PCR.Nucleic Acids Research, 29, e45. |
[30] | Phillips JM, Hayman DS (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection.Transactions of the British Mycological Society, 55, 158-161. |
[31] | Plénet D, Etchebest S, Mollier A, Pellerin S (2000). Growth analysis of maize field crops under phosphorus deficiency.Plant and Soil, 223, 119-132. |
[32] | Radchuk R, Radchuk V, G?tz KP, Weichert H, Richter A, Emery RJ, Winfriede W, Weber H (2007). Ectopic expression of phosphoenolpyruvate carboxylase in Vicia narbonensis seeds: Effects of improved nutrient status on seed maturation and transcriptional regulatory networks.The Plant Journal, 51, 819-839. |
[33] | Ramaiah M, Jain A, Baldwin JC, Karthikeyan AS, Raghothama KG (2011). Characterization of the phosphate starvation- induced glycerol-3-phosphate permease gene family inArabidopsis. Plant physiology, 157, 279-291. |
[34] | Rich MK, Schorderet M, Reinhardt D (2014). The role of the cell wall compartment in mutualistic symbioses of plants.Frontiers in Plant Science, 5, 238. |
[35] | Rojas-Beltrán JA, Dubois F, Mortiaux F, Portetelle D, Gebhardt C, Sangwan RS, du Jardin P (1999). Identification of cytosolic Mg2+-dependent soluble inorganic pyrophosphatases in potato and phylogenetic analysis.Plant Molecular Biology, 39, 449-461. |
[36] | Rolletschek H, Borisjuk L, Radchuk R, Miranda M, Heim U, Wobus U, Weber H (2004). Seed-specific expression of a bacterial phosphoenolpyruvate carboxylase in Vicia narbonensis increases protein content and improves carbon economy.Plant Biotechnology Journal, 2, 211-219. |
[37] | Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009). The B73 maize genome: Complexity, diversity, and dynamics.Science, 326, 1112-1115. |
[38] | Smith SE, Read DJ (2008). Arbuscular mycorrhizas.Mycorrhizal Symbiosis, 3, 11-145. |
[39] | Tyler G (1999). Plant distribution and soil-plant interactions on shallow soils.Acta Phytogeographica Suecica, 84, 21-32. |
[40] | van der Heijden MGA, Horton TR (2009). Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems.Journal of Ecology, 97, 1139-1150. |
[41] | Wright DP, Read DJ, Scholes JD (1998). Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L.Plant, Cell & Environment, 21, 881-891. |
[42] | Yoshihiro K, Miki K, Katsuharu S, Kikuchi Y, Ezawa T, Maeshima M, Hata S, Fujiwara T (2015). Up-regulation of genes involved in N-acetylglucosamine uptake and metabolism suggests a recycling mode of chitin in intraradical mycelium of arbuscular mycorrhizal fungi.Mycorrhiza, 25, 411-417. |
/
〈 |
|
〉 |