| Citation: |
XIONG Zhen-Gui, LIU Zheng-Han, SONG Chun-Lei, AO Zi-Qiang, CAO Xiu-Yun. ECOLOGICAL SIGNIFICANCE AND RESEARCH PROGRESS OF CYANOBACTERIAL BLOOMS RESPONDING TO LOW PHOSPHORUS STRESS BY REPLACING PHOSPHOLIPIDS WITH NON-PHOSPHOLIPIDS[J]. ACTA HYDROBIOLOGICA SINICA. DOI: 10.7541/2025.2025.0043
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Freshwater cyanobacterial blooms occur globally, with phosphorus (P) being a key limiting nutrient for cyanobacterial growth and proliferation. Eutrophication is widely recognized as the primary driver of cyanobacterial dominance. However, even under extremely low phosphorus conditions, cyanobacteria can maintain high biomass levels. A potential intrinsic mechanism involves their ability to substitute phospholipids with non-phosphorus lipids (e.g., sulfolipids and glycolipids), thereby reducing cellular phosphorus demand and overcoming P limitation, which grants them a competitive advantage to form blooms. This review synthesizes strategies employed by typical bloom-forming cyanobacteria to regulate lipid metabolism under phosphorus stress, particularly through replacing phospholipids (e.g., phosphatidylglycerol, PG) with sulfolipids (e.g., sulfoquinovosyldiacylglycerol, SQDG) and glycolipids (e.g., monogalactosyldiacylglycerol, MGDG; digalactosyldiacylglycerol, DGDG). The ecological implications of this adaptation mechanism are critically examined. By unveiling novel phosphorus-sparing strategies in cyanobacteria, this study provides new insights into the mechanisms driving bloom formation and proposes innovative approaches for bloom control. This is particularly significant given that current prevention and control methods primarily focus on reducing nutrient loads, underscoring the need to revisit conventional eutrophication management paradigms.
| [1] |
孔繁翔, 高光. 大型浅水富营养化湖泊中蓝藻水华形成机理的思考 [J]. 生态学报, 2005, 25(3): 589-595.] doi: 10.3321/j.issn:1000-0933.2005.03.028
Kong F X, Gao G. Hypothesis on cyanobacteria bloom-forming mechanism in large shallow eutrophic lakes [J]. Acta Ecologica Sinica, 2005, 25(3): 589-595. [ doi: 10.3321/j.issn:1000-0933.2005.03.028
|
| [2] |
秦伯强, 王小冬, 汤祥明, 等. 太湖富营养化与蓝藻水华引起的饮用水危机——原因与对策 [J]. 地球科学进展, 2007, 22(9): 896-906.] doi: 10.3321/j.issn:1001-8166.2007.09.003
Qin B Q, Wang X D, Tang X M, et al. Drinking water crisis caused by eutrophication and cyanobacterial bloom in Lake Taihu: cause and measurement [J]. Advances in Earth Science, 2007, 22(9): 896-906. [ doi: 10.3321/j.issn:1001-8166.2007.09.003
|
| [3] |
Qin B, Gao G, Zhu G, et al. Lake eutrophication and its ecosystem response [J]. Chinese Science Bulletin, 2013, 58(9): 961-970.
|
| [4] |
Geng M, Zhang W, Hu T, et al. Eutrophication causes microbial community homogenization via modulating generalist species [J]. Water Research, 2022(210): 118003.
|
| [5] |
Jochimsen E M, Carmichael W W, An J S, et al. Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil [J]. The New England Journal of Medicine, 1998, 338(13): 873-878.
|
| [6] |
Lee K L, Jung K Y, et al. Effect of nitrogen and phosphorus on growth and microcystin production in three Microcystis species [J]. Journal of Environmental Biology, 2018, 39(4): 413-418.
|
| [7] |
Chia M A, Jankowiak J G, Kramer B J, et al. Succession and toxicity of Microcystis and Anabaena (Dolichospermum) blooms are controlled by nutrient-dependent allelopathic interactions [J]. Harmful Algae, 2018(74): 67-77.
|
| [8] |
Qian Y P, Li X T, Tian R N. Effects of aqueous extracts from the rhizome of Pontederia cordata on the growth and interspecific competition of two algal species [J]. Ecotoxicology and Environmental Safety, 2019(168): 401-407.
|
| [9] |
Fei X, Li P, Li X, et al. Low-temperature- and phosphate deficiency-responsive elements control DGTT3 expression in Chlamydomonas reinhardtii [J]. Journal of Eukaryotic Microbiology, 2018, 65(1): 117-126.
|
| [10] |
Hałemejko G Z, Chróst R. The role of phosphatases in phosphorus mineralization during decomposition of lake phytoplankton blooms [J]. Archiv Fur Hydrobiologie, 1984(101): 489-502.
|
| [11] |
朱广伟, 秦伯强, 高光, 等. 长江中下游浅水湖泊沉积物中磷的形态及其与水相磷的关系 [J]. 环境科学学报, 2004, 24(3): 381-388.] doi: 10.3321/j.issn:0253-2468.2004.03.003
Zhu G W, Qin B Q, Gao G, et al. Fractionation of phosphorus in sediments and its relation with soluble phosphorus contents in shallow lakes located in the middle and lower reaches of Changjiang River, China [J]. Acta Scientiae Circumstantiae, 2004, 24(3): 381-388. [ doi: 10.3321/j.issn:0253-2468.2004.03.003
|
| [12] |
Surin B P, Rosenberg H, Cox G B. Phosphate-specific transport system of Escherichia coli: nucleotide sequence and gene-polypeptide relationships [J]. Journal of Bacteriology, 1985, 161(1): 189-198.
|
| [13] |
Dyhrman S T, Jenkins B D, Rynearson T A, et al. The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response [J]. PLoS One, 2012, 7(3): e33768.
|
| [14] |
McLaughlin K, Sohm J A, Cutter G A, et al. Phosphorus cycling in the sargasso sea: investigation using the oxygen isotopic composition of phosphate, enzyme-labeled fluorescence, and turnover times [J]. Global Biogeochemical Cycles, 2013, 27(2): 375-387.
|
| [15] |
Van Mooy B A S, Rocap G, Fredricks H F, et al. Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments [J]. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(23): 8607-8612.
|
| [16] |
Peng Z, Feng L, Wang X, et al. Adaptation of Synechococcus sp. PCC 7942 to phosphate starvation by glycolipid accumulation and membrane lipid remodeling [J]. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids, 2019, 1864(12): 158522.
|
| [17] |
Ho J C, Michalak A M, Pahlevan N. Widespread global increase in intense lake phytoplankton blooms since the 1980s [J]. Nature, 2019, 574(7780): 667-670.
|
| [18] |
Sukharevich V I, Polyak Y M. Global occurrence of cyanobacteria: causes and effects (review) [J]. Inland Water Biology, 2020, 13(4): 566-575.
|
| [19] |
Petkuviene J, Zilius M, Lubiene I, et al. Phosphorus cycling in a freshwater estuary impacted by cyanobacterial blooms [J]. Estuaries and Coasts, 2016, 39(5): 1386-1402.
|
| [20] |
Huo D, Gan N, Geng R, et al. Cyanobacterial blooms in China: diversity, distribution, and cyanotoxins [J]. Harmful Algae, 2021(109): 102106.
|
| [21] |
Ndlela L L, Oberholster P J, Van Wyk J H, et al. An overview of cyanobacterial bloom occurrences and research in Africa over the last decade [J]. Harmful Algae, 2016(60): 11-26.
|
| [22] |
Massey I Y, Al osman M, Yang F. An overview on cyanobacterial blooms and toxins production: their occurrence and influencing factors [J]. Toxin Reviews, 2022, 41(1): 326-346.
|
| [23] |
杨柳燕, 杨欣妍, 任丽曼, 等. 太湖蓝藻水华暴发机制与控制对策 [J]. 湖泊科学, 2019, 31(1): 18-27.] doi: 10.18307/2019.0102
Yang L Y, Yang X Y, Ren L M, et al. Mechanism and control strategy of cyanobacterial bloom in Lake Taihu [J]. Journal of Lake Sciences, 2019, 31(1): 18-27. [ doi: 10.18307/2019.0102
|
| [24] |
许海, 陈洁, 朱广伟, 等. 水体氮、磷营养盐水平对蓝藻优势形成的影响 [J]. 湖泊科学, 2019, 31(5): 1239-1247.] doi: 10.18307/2019.0518
Xu H, Chen J, Zhu G W, et al. Effect of concentrations of phosphorus and nitrogen on the dominance of cyanobacteria [J]. Journal of Lake Sciences, 2019, 31(5): 1239-1247. [ doi: 10.18307/2019.0518
|
| [25] |
Salmaso N, Capelli C, Shams S, et al. Expansion of bloom-forming Dolichospermum lemmermannii (Nostocales, Cyanobacteria) to the deep lakes south of the Alps: Colonization patterns, driving forces and implications for water use [J]. Harmful Algae, 2015(50): 76-87.
|
| [26] |
Sterner R W, Reinl K L, Lafrancois B M, et al. A first assessment of cyanobacterial blooms in oligotrophic Lake Superior [J]. Limnology and Oceanography, 2020, 65(12): 2984-2998.
|
| [27] |
Molot L A, Schiff S L, Venkiteswaran J J, et al. Low sediment redox promotes cyanobacteria blooms across a trophic range: implications for management [J]. Lake and Reservoir Management, 2021, 37(2): 120-142.
|
| [28] |
Reinl K L, Brookes J D, Carey C C, et al. Cyanobacterial blooms in oligotrophic lakes: shifting the high-nutrient paradigm [J]. Freshwater Biology, 2021, 66(9): 1846-1859.
|
| [29] |
Lefler F W, Barbosa M, Zimba P V, et al. Spatiotemporal diversity and community structure of cyanobacteria and associated bacteria in the large shallow subtropical Lake Okeechobee (Florida, United States) [J]. Frontiers in Microbiology, 2023(14): 1219261.
|
| [30] |
Smith V H, Wood S A, McBride C G, et al. Phosphorus and nitrogen loading restraints are essential for successful eutrophication control of Lake Rotorua, New Zealand [J]. Inland Waters, 2016, 6(2): 273-283.
|
| [31] |
Wu P, Lu Y, Lu Y, et al. Response of the photosynthetic activity and biomass of the phytoplankton community to increasing nutrients during cyanobacterial blooms in Meiliang Bay, Lake Taihu [J]. Water Environment Research, 2020, 92(1): 138-148.
|
| [32] |
Wei N, Chen A, Guo X, et al. Changes in nitrogen metabolism of phosphorus-starved bloom-forming Cyanobacterium Microcystis aeruginosa: Implications for nutrient management [J]. Science of the Total Environment, 2023(903): 166832.
|
| [33] |
Liang Z, Soranno P A, Wagner T. The role of phosphorus and nitrogen on chlorophyll a: Evidence from hundreds of lakes [J]. Water Research, 2020(185): 116236.
|
| [34] |
Ghaffar S, Stevenson R J, Khan Z. Effect of phosphorus stress on Microcystis aeruginosa growth and phosphorus uptake [J]. PLoS One, 2017, 12(3): e0174349.
|
| [35] |
Paerl H W, Otten T G. Harmful cyanobacterial blooms: causes, consequences, and controls [J]. Microbial Ecology, 2013, 65(4): 995-1010.
|
| [36] |
Tonetta D, Hennemann M C, Brentano D M, et al. Considerations regarding the dominance of Cylindrospermopsis raciborskii under low light availability in a low phosphorus lake [J]. Acta Botanica Brasilica, 2015, 29(3): 448-451.
|
| [37] |
Paerl H W, Huisman J. Blooms like it hot [J]. Science), 2008, 320(5872): 57-58.
|
| [38] |
Briddon C L, Szekeres E, Hegedüs A, et al. The combined impact of low temperatures and shifting phosphorus availability on the competitive ability of cyanobacteria [J]. Scientific Reports, 2022, 12(1): 16409.
|
| [39] |
Qiu G W, Zheng W C, Yang H M, et al. Phosphorus deficiency alleviates iron limitation in Synechocystis cyanobacteria through direct PhoB-mediated gene regulation [J]. Nature Communications, 2024, 15(1): 4426.
|
| [40] |
Li J, Wang Z, Cao X, et al. Effect of orthophosphate and bioavailability of dissolved organic phosphorous compounds to typically harmful Cyanobacterium Microcystis aeruginosa [J]. Marine Pollution Bulletin, 2015, 92(1/2): 52-58.
|
| [41] |
Dyhrman S, Ammerman J, Van Mooy B. Microbes and the marine phosphorus cycle [J]. Oceanography, 2007, 20(2): 110-116.
|
| [42] |
Harke M J, Berry D L, Ammerman J W, et al. Molecular response of the bloom-forming Cyanobacterium, Microcystis aeruginosa, to phosphorus limitation [J]. Microbial Ecology, 2012, 63(1): 188-198.
|
| [43] |
Xiao M, Burford M A, Prentice M J, et al. Phosphorus storage and utilization strategies of two bloom-forming freshwater cyanobacteria [J]. Proceedings Biological Sciences, 2023, 290(2003): 20231204.
|
| [44] |
Pitt F D, Mazard S, Humphreys L, et al. Functional characterization of Synechocystis sp. strain PCC 6803 pst1 and pst2 gene clusters reveals a novel strategy for phosphate uptake in a freshwater Cyanobacterium [J]. Journal of Bacteriology, 2010, 192(13): 3512-3523.
|
| [45] |
Wan L, Chen X, Deng Q, et al. Phosphorus strategy in bloom-forming cyanobacteria (Dolichospermum and Microcystis) and its role in their succession [J]. Harmful Algae, 2019(84): 46-55.
|
| [46] |
Shi X, Yang L, Niu X, et al. Intracellular phosphorus metabolism of Microcystis aeruginosa under various redox potential in darkness [J]. Microbiological Research, 2003, 158(4): 345-352.
|
| [47] |
Wang M, Zhan Y, Chen C, et al. Amplified cyanobacterial bloom is derived by polyphosphate accumulation triggered by ultraviolet light [J]. Water Research, 2022(222): 118837.
|
| [48] |
Van Mooy B A S, Fredricks H F, Pedler B E, et al. Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity [J]. Nature, 2009, 458(7234): 69-72.
|
| [49] |
Peng G, Lin S, Fan Z, et al. Transcriptional and physiological responses to nutrient loading on toxin formation and photosynthesis in Microcystis aeruginosa FACHB-905 [J]. Toxins, 2017, 9(5): 168. doi: 10.3390/toxins9050168
|
| [50] |
Peng G, Wilhelm S W, Lin S, et al. Response of Microcystis aeruginosa FACHB-905 to different nutrient ratios and changes in phosphorus chemistry [J]. Journal of Oceanology and Limnology, 2018, 36(4): 1040-1052.
|
| [51] |
Duan Z, Tan X, Paerl H W, et al. Ecological stoichiometry of functional traits in a colonial harmful Cyanobacterium [J]. Limnology and Oceanography, 2021, 66(5): 2051-2062.
|
| [52] |
Duan Z, Tan X, Shi L, et al. Phosphorus accumulation in extracellular polymeric substances (EPS) of colony-forming cyanobacteria challenges imbalanced nutrient reduction strategies in eutrophic lakes [J]. Environmental Science & Technology, 2023, 57(4): 1600-1612.
|
| [53] |
Lin S, Litaker R W, Sunda W G. Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton [J]. Journal of Phycology, 2016, 52(1): 10-36.
|
| [54] |
Xiao M, Burford M A, Wood S A, et al. Schindler’s legacy: from eutrophic lakes to the phosphorus utilization strategies of cyanobacteria [J]. FEMS Microbiology Reviews, 2022, 46(6): fuac029.
|
| [55] |
Thompson G A. Lipids and membrane function in green algae [J]. Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, 1996, 1302(1): 17-45.
|
| [56] |
Jahns P, Latowski D, Strzalka K. Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids [J]. Biochimica et Biophysica Acta(BBA)-Bioenergetics, 2009, 1787(1): 3-14.
|
| [57] |
Singh S, Sinha R P, Haeder D P. Role of lipids and fatty acids in stress tolerance in cyanobacteria [J]. Acta Protozoologica, 2002(41): 297-308.
|
| [58] |
Domonkos I, Laczkó-Dobos H, Gombos Z. Lipid-assisted protein–protein interactions that support photosynthetic and other cellular activities [J]. Progress in Lipid Research, 2008, 47(6): 422-435.
|
| [59] |
Weier D, Müller C, Gaspers C, et al. Characterisation of acyltransferases from Synechocystis sp. PCC6803 [J]. Biochemical and Biophysical Research Communications, 2005, 334(4): 1127-1134.
|
| [60] |
Demé B, Cataye C, Block M A, et al. Contribution of galactoglycerolipids to the 3-dimensional architecture of thylakoids [J]. The FASEB Journal, 2014, 28(8): 3373-3383.
|
| [61] |
Bertilsson S, Berglund O, Karl D M, et al. Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea [J]. Limnology and Oceanography, 2003, 48(5): 1721-1731.
|
| [62] |
Shemi A, Schatz D, Fredricks H F, et al. Phosphorus starvation induces membrane remodeling and recycling in Emiliania huxleyi [J]. New Phytologist, 2016, 211(3): 886-898. doi: 10.1111/nph.13940
|
| [63] |
Peng Z, Miao X. Monoglucosyldiacylglycerol participates in phosphate stress adaptation in Synechococcus sp. PCC 7942 [J]. Biochemical and Biophysical Research Communications, 2020, 522(3): 662-668.
|
| [64] |
Aoki M, Sato N, Meguro A, et al. Differing involvement of sulfoquinovosyl diacylglycerol in photosystem II in two species of unicellular cyanobacteria [J]. European Journal of Biochemistry, 2004, 271(4): 685-693.
|
| [65] |
Nakajima Y, Umena Y, Nagao R, et al. Thylakoid membrane lipid sulfoquinovosyl-diacylglycerol (SQDG) is required for full functioning of photosystem II in Thermosynechococcus elongatus [J]. Journal of Biological Chemistry, 2018, 293(38): 14786-14797.
|
| [66] |
Kobayashi K, Fujii S, Sato M, et al. Specific role of phosphatidylglycerol and functional overlaps with other thylakoid lipids in Arabidopsis chloroplast biogenesis [J]. Plant Cell Reports, 2015, 34(4): 631-642.
|
| [67] |
Hung C H, Endo K, Kobayashi K, et al. Characterization of Chlamydomonas reinhardtii phosphatidylglycerophosphate synthase in Synechocystis sp. PCC 6803 [J]. Frontiers in Microbiology, 2015(6): 842.
|
| [68] |
Song Y, Li R, Song W, et al. Microcystis spp. and phosphorus in aquatic environments: a comprehensive review on their physiological and ecological interactions [J]. The Science of the Total Environment, 2023 (878): 163136.
|
| [69] |
Xu X, Miao X. Glyceroglycolipid metabolism regulations under phosphate starvation revealed by transcriptome analysis in Synechococcus elongatus PCC 7942 [J]. Marine Drugs, 2020, 18(7): 360.
|
| [70] |
Hassan M J, Qi H, Cheng B, et al. Enhanced adaptability to limited water supply regulated by diethyl aminoethyl hexanoate (DA-6) associated with lipidomic reprogramming in two white clover genotypes [J]. Frontiers in Plant Science, 2022(13): 879331.
|
| [71] |
Sun Y, Song K, Liu L, et al. Sulfoquinovosyl diacylglycerol synthase 1 impairs glycolipid accumulation and photosynthesis in phosphate-deprived rice [J]. Journal of Experimental Botany, 2021, 72(18): 6510-6523.
|
| [72] |
Liebisch T, Başoglu M, Jäger S, et al. Influence of reduced amounts of sulfoquinovosyl diacylglycerol on the thylakoid membranes of the diatom Thalassiosira pseudonana [J]. Photosynthetica, 2023, 61(4): 425-431.
|
| [73] |
Liu Z, Wan L, Zhang J, et al. A novel strategy of bloom forming cyanobacteria Microcystis sp. in response to phosphorus deficiency: Using non-phosphorus lipids substitute phospholipids [J]. Harmful Algae, 2024(138): 102694.
|
| [74] |
Martin R M, Denney M K, Pound H L, et al. Sulfolipid substitution ratios of Microcystis aeruginosa and planktonic communities as an indicator of phosphorus limitation in Lake Erie [J]. Limnology and Oceanography, 2023, 68(5): 1117-1131.
|
| [75] |
Endo K, Kobayashi K, Wada H. Sulfoquinovosyldiacylglycerol has an essential role in Thermosynechococcus elongatus BP-1 under phosphate-deficient conditions [J]. Plant & Cell Physiology, 2016, 57(12): 2461-2471.
|
| [76] |
Bagnato C, Prados M B, Franchini G R, et al. Analysis of triglyceride synthesis unveils a green algal soluble diacylglycerol acyltransferase and provides clues to potential enzymatic components of the chloroplast pathway [J]. BMC Genomics, 2017, 18(1): 223.
|
| [77] |
Peng Z, Miao X. Monoglucosyldiacylglycerol participates in phosphate stress adaptation in Synechococcus sp. PCC 7942 [J]. Biochemical and Biophysical Research Communications, 2020, 522(3): 662-668.
|
| [78] |
Sato N, Ebiya Y, Kobayashi R, et al. Disturbance of cell-size determination by forced overproduction of sulfoquinovosyl diacylglycerol in the Cyanobacterium Synechococcus elongatus PCC 7942 [J]. Biochemical and Biophysical Research Communications, 2017, 487(3): 734-739.
|
| [79] |
Sato N, Kamimura R, Tsuzuki M. Dispensability of a sulfolipid for photoautotrophic cell growth and photosynthesis in a marine Cyanobacterium, Synechococcus sp. PCC 7002 [J]. Biochemical and Biophysical Research Communications, 2016, 477(4): 854-860. doi: 10.1016/j.bbrc.2016.06.148
|
| [80] |
Cumino A C, Marcozzi C, Barreiro R, et al. Carbon cycling in Anabaena sp. PCC 7120. Sucrose synthesis in the heterocysts and possible role in nitrogen fixation [J]. Plant Physiology, 2007, 143(3): 1385-1397. doi: 10.1104/pp.106.091736
|
| [81] |
Malatinszky D, Steuer R, Jones P R. A comprehensively curated genome-scale two-cell model for the heterocystous Cyanobacterium anabaena sp. PCC 7120 [J]. Plant Physiology, 2017, 173(1): 509-523. doi: 10.1104/pp.16.01487
|
| [82] |
Gollan P J, Muth-Pawlak D, Aro E-M. Rapid transcriptional reprogramming triggered by alteration of the carbon/nitrogen balance has an impact on energy metabolism in Nostoc sp. PCC 7120 [J]. Life, 2020, 10(11): 297. doi: 10.3390/life10110297
|
| [83] |
Roumezi B, Xu X, Risoul V, et al. The Pkn22 kinase of Nostoc PCC 7120 is required for cell differentiation via the phosphorylation of HetR on a residue highly conserved in genomes of heterocyst-forming cyanobacteria [J]. Frontiers in Microbiology, 2019(10): 3140.
|
| [84] |
Dolman A M, Rücker J, Pick F R, et al. Cyanobacteria and cyanotoxins: the influence of nitrogen versus phosphorus [J]. PLoS One, 2012, 7(6): e38757. doi: 10.1371/journal.pone.0038757
|
| [85] |
Zhang Q, Jia L, Chen Y, et al. Molecular mechanisms of the cyanobacterial response to different phosphorus sources [J]. Sustainability, 2024, 16(13): 5642. doi: 10.3390/su16135642
|
| [86] |
Aubriot L. Nitrogen availability facilitates phosphorus acquisition by bloom-forming cyanobacteria [J]. FEMS Microbiology Ecology, 2019, 95(2): 5195515.
|
| [87] |
Yang B, Li M, Phillips A, et al. Nonspecific phospholipase C4hydrolyzes phosphosphingolipids and sustains plant root growth during phosphate deficiency [J]. The Plant Cell, 2021, 33(3): 766-780. doi: 10.1093/plcell/koaa054
|
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| |
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|
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