Diversity of Arbuscular Mycorrhizal Fungi Associated with Six Rice Cultivars in Italian Agricultural Ecosystem Managed with Alternate Wetting and Drying
Received date: 2022-11-08
Accepted date: 2023-02-23
Online published: 2023-03-13
Alternate wetting and drying (AWD) system, in which water has been reduced by approximately 35% with an increased occurrence of beneficial arbuscular mycorrhizal (AM) symbiosis and no negative impact on rice yield, was proposed to utilize water and nutrients more sustainable. In this study, we selected six rice cultivars (Centauro, Loto, Selenio, Vialone nano, JSendra and Puntal) grown under AWD conditions, and investigated their responsiveness to AM colonization and how they select diverse AM taxa. In order to investigate root-associated AM fungus communities, molecular cloning-Sanger sequencing on small subunit rDNA data were obtained from five out of the six rice cultivars and compared with Next Generation Sequencing (NGS) data, which were previously obtained in Vialone nano. The results showed that all the cultivars were responsive to AM colonization with the development of AM symbiotic structures, even if with differences in the colonization and arbuscule abundance in the root systems. We identified 16 virtual taxa (VT) in the soil compartment and 7 VT in the root apparatus. We emphasized that the NGS analysis gives additional value to the results thanks to a more in-depth reading of the less represented AM fungus taxa.
Veronica Volpe, Franco Magurno, Paola Bonfante, Stefano Ghignone, Erica Lumini . Diversity of Arbuscular Mycorrhizal Fungi Associated with Six Rice Cultivars in Italian Agricultural Ecosystem Managed with Alternate Wetting and Drying[J]. Rice Science, 2023 , 30(4) : 348 -358 . DOI: 10.1016/j.rsci.2023.02.003
| [1] | Abadi S, Azouri D, Pupko T, Mayrose I. 2019. Model selection may not be a mandatory step for phylogeny reconstruction. Nat Commun, 10(1): 934. |
| [2] | Arnault G, Mony C, Vandenkoornhuyse P. 2023. Plant microbiota dysbiosis and the Anna Karenina Principle. Trends Plant Sci, 28: 18-30. |
| [3] | Bago B, Pfeffer P E, Shachar-Hill Y. 2000. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol, 124(3): 949-958. |
| [4] | Bao X Z, Wang Y T, Olsson P A. 2019. Arbuscular mycorrhiza under water: Carbon-phosphorus exchange between rice and arbuscular mycorrhizal fungi under different flooding regimes. Soil Biol Biochem, 129: 169-177. |
| [5] | Berger S A, Krompass D, Stamatakis A. 2011. Performance, accuracy, and Web server for evolutionary placement of short sequence reads under maximum likelihood. Syst Biol, 60(3): 291-302. |
| [6] | Bernaola L, Cange G, Way M O, Gore J, Hardke J, Stout M. 2018. Natural colonization of rice by arbuscular mycorrhizal fungi in different production areas. Rice Sci, 25(3): 169-174. |
| [7] | Bin Rahman A N M R, Zhang J H. 2023. Trends in rice research: 2030 and beyond. Food Energy Secur, 12: e390. |
| [8] | B?aszkowski J, Koz?owska A, Niezgoda P, Goto B T, Dalpé Y. 2018a. A new genus, Oehlia with Oehlia diaphana comb. nov. and an emended description of Rhizoglomus vesiculiferum comb. nov. in the Glomeromycotina. Nova Hedwigia, 107(3/4): 501-518. |
| [9] | B?aszkowski J, Niezgoda P, Goto B T, Koz?owska A. 2018b. Halonatospora Gen. nov. with H. pansihalos comb. nov. and Glomus bareae sp. nov. (Glomeromycota; Glomeraceae). Botany, 96(11): 737-748. |
| [10] | B?aszkowski J, Jobim K, Niezgoda P, Meller E, Malinowski R, Milczarski P, Zubek S, Magurno F, Casieri L, Bierza W, B?aszkowski T, Crossay T, Goto B T. 2021. New Glomeromycotan taxa, Dominikia glomerocarpica sp. nov. and Epigeocarpum crypticum gen. nov. et sp. nov. from Brazil, and Silvaspora gen. nov. from New Caledonia. Front Microbiol, 12: 655910. |
| [11] | Bouman B A M, Tuong T P. 2001. Field water management to save water and increase its productivity in irrigated lowland rice. Agric Water Manag, 49(1): 11-30. |
| [12] | Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden T L. 2009. BLAST+: Architecture and applications. BMC Bioinformatics, 10: 421. |
| [13] | Campo S, Martín-Cardoso H, Olivé M, Pla E, Catala-Forner M, Martínez-Eixarch M, Segundo B S. 2020. Effect of root colonization by arbuscular mycorrhizal fungi on growth, productivity and blast resistance in rice. Rice, 13(1): 42. |
| [14] | Campos-Soriano L, García-Martínez J, Segundo B S. 2012. The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol, 13(6): 579-592. |
| [15] | Caporaso J G, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, Costello E K, Fierer N, Pe?a A G, Goodrich J K, Gordon J I, Huttley G A, Kelley S T, Knights D, Koenig J E, Ley R E, Lozupone C A, McDonald D, Muegge B D, Pirrung M, Reeder J, Sevinsky J R, Turnbaugh P J, Walters W A, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods, 7(5): 335-336. |
| [16] | Carballar-Hernández S, Hernández-Cuevas L V, Monta?o N M, Larsen J, Ferrera-Cerrato R, Taboada-Gaytán O R, Montiel- González A M, Alarcón A. 2017. Native communities of arbuscular mycorrhizal fungi associated with Capsicum annuum L. respond to soil properties and agronomic management under field conditions. Agric Ecosyst Environ, 245: 43-51. |
| [17] | Cardoso C, Zhang Y X, Jamil M, Hepworth J, Charnikhova T, Dimkpa S O N, Meharg C, Wright M H, Liu J W, Meng X B, Wang Y H, Li J Y, McCouch S R, Leyser O, Price A H, Bouwmeester H J, Ruyter-Spira C. 2014. Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs. Proc Natl Acad Sci USA, 111(6): 2379-2384. |
| [18] | Casazza G, Lumini E, Ercole E, Dovana F, Guerrina M, Arnulfo A, Minuto L, Fusconi A, Mucciarelli M. 2017. The abundance and diversity of arbuscular mycorrhizal fungi are linked to the soil chemistry of screes and to slope in the Alpic paleo-endemic Berardia subacaulis. PLoS One, 12(2): e0171866. |
| [19] | Chen X W, Wu F Y, Li H, Chan W F, Wu S C, Wong M H. 2017. Mycorrhizal colonization status of lowland rice (Oryza sativa L.) in the southeastern region of China. Environ Sci Pollut Res, 24(6): 5268-5276. |
| [20] | Chialva M, Ghignone S, Cozzi P, Lazzari B, Bonfante P, Abbruscato P, Lumini E. 2020. Water management and phenology influence the root-associated rice field microbiota. FEMS Microbiol Ecol, 96(9): fiaa146. |
| [21] | Chiu C H, Choi J, Paszkowski U. 2018. Independent signalling cues underpin arbuscular mycorrhizal symbiosis and large lateral root induction in rice. New Phytol, 217(2): 552-557. |
| [22] | Corazon-Guivin M A, Cerna-Mendoza A, Guerrero-Abad J C, Vallejos-Tapullima A, Carballar-Hernández S, Alves da Silva G, Oehl F. 2019a. Nanoglomus plukenetiae, a new fungus from Peru, and a key to small-spored Glomeraceae species, including three new genera in the ‘Dominikia complex/clades’. Mycol Prog, 18(12): 1395-1409. |
| [23] | Corazon-Guivin M A, Mendoza A C, Guerrero-Abad J C, Vallejos- Tapullima A, Carballar-Hernández S, da Silva G A, Oehl F. 2019b. Funneliglomus gen. nov., and Funneliglomus sanmartinensis, a new arbuscular mycorrhizal fungus from the Amazonia region in Peru. Sydowia, 71: 17-24. |
| [24] | Czech L, Barbera P, Stamatakis A. 2020. Genesis and Gappa: Processing, analyzing and visualizing phylogenetic (placement) data. Bioinformatics, 36(10): 3263-3265. |
| [25] | da Silva K J G, Fernandes J A L, Magurno F, Leandro L B A, Goto B T, Theodoro R C. 2022. Phylogenetic review of Acaulospora (Diversisporales, Glomeromycota) and the homoplasic nature of its ornamentations. J Fungi, 8(9): 892. |
| [26] | Davidson H, Shrestha R, Cornulier T, Douglas A, Travis T, Johnson D, Price A H. 2019. Spatial effects and GWA mapping of root colonization assessed in the interaction between the rice diversity panel 1 and an arbuscular mycorrhizal fungus. Front Plant Sci, 10: 633. |
| [27] | Diedhiou A G, Mbaye F K, Mbodj D, Faye M N, Pignoly S, Ndoye I, Djaman K, Gaye S, Kane A, Laplaze L, Manneh B, Champion A. 2016. Field trials reveal ecotype-specific responses to mycorrhizal inoculation in rice. PLoS One, 11(12): e0167014. |
| [28] | Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty N K, Bhatnagar S, Eisen J A, Sundaresan V. 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA, 112(8): E911-E920. |
| [29] | Fiorilli V, Vallino M, Biselli C, Faccio A, Bagnaresi P, Bonfante P. 2015. Host and non-host roots in rice: Cellular and molecular approaches reveal differential responses to arbuscular mycorrhizal fungi. Front Plant Sci, 6: 636. |
| [30] | Genre A, Lanfranco L, Perotto S, Bonfante P. 2020. Unique and common traits in mycorrhizal symbioses. Nat Rev Microbiol, 18(11): 649-660. |
| [31] | Gewaily S. 2019. Influence of arbuscular mycorrhizal (AMF) inoculation on the performance of Sakha 107 rice cultivar under different irrigation intervals. Environ Biodivers Soil Secur, 3: 119-130. |
| [32] | Goncharova J K, Kharitonov E M. 2016. Genetic control of traits associated with phosphorus uptake in rice (Oryza sativa L.) varieties. Russ J Genet Appl Res, 6(3): 270-278. |
| [33] | Hart M M, Reader R J. 2002. Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol, 153(2): 335-344. |
| [34] | Hempel S, Renker C, Buscot F. 2007. Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol, 9(8): 1930-1938. |
| [35] | Huang R L, Li Z, Shen X H, Choi J, Cao Y R. 2022. The perspective of arbuscular mycorrhizal symbiosis in rice domestication and breeding. Int J Mol Sci, 23(20): 12383. |
| [36] | Ibne Baki M Z, Suzuki K, Takahashi K, Chowdhury S A, Asiloglu R, Harada N. 2021. Molecular genetic characterization of arbuscular mycorrhizal fungi associated with upland rice in Bangladesh. Rhizosphere, 18: 100357. |
| [37] | Jobim K, B?aszkowski J, Niezgoda P, Koz?owska A, Zubek S, Mleczko P, Chachu?a P, Ishikawa N K, Goto B T. 2019. New sporocarpic taxa in the phylum Glomeromycota: Sclerocarpum amazonicum gen. et sp. nov. in the family Glomeraceae (Glomerales) and Diversispora sporocarpia sp. nov. in the Diversisporaceae (Diversisporales). Mycol Prog, 18(3): 369-384. |
| [38] | Katoh K, Standley D M. 2013. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol, 30(4): 772-780. |
| [39] | Keymer A, Pimprikar P, Wewer V, Huber C, Brands M, Bucerius S L, Delaux P M, Klingl V, R?penack-Lahaye E V, Wang T L, Eisenreich W, D?rmann P, Parniske M, Gutjahr C. 2017. Lipid transfer from plants to arbuscular mycorrhiza fungi. eLife, 6: e29107. |
| [40] | Kozlov A M, Darriba D, Flouri T, Morel B, Stamatakis A. 2019. RAxML-NG: A fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics, 35(21): 4453-4455. |
| [41] | Krüger M, Krüger C, Walker C, Stockinger H, Schü?ler A. 2012. Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol, 193(4): 970-984. |
| [42] | Lampayan R M, Rejesus R M, Singleton G R, Bouman B A M. 2015. Adoption and economics of alternate wetting and drying water management for irrigated lowland rice. Field Crops Res, 170: 95-108. |
| [43] | Lancashire P D, Bleiholder H, van den Boom T, Langelüddeke P, Stauss R, Weber E, Witzenberger A. 1991. A uniform decimal code for growth stages of crops and weeds. Ann Appl Biol, 119(3): 561-601. |
| [44] | Lanfranco L, Fiorilli V, Venice F, Bonfante P. 2018. Strigolactones cross the kingdoms: Plants, fungi, and bacteria in the arbuscular mycorrhizal symbiosis. J Exp Bot, 69(9): 2175-2188. |
| [45] | Lee J, Lee S S. 2008. Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol, 65(2): 339-349. |
| [46] | Luginbuehl L H, Menard G N, Kurup S, van Erp H, Radhakrishnan G V, Breakspear A, Oldroyd G E D, Eastmond P J. 2017. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science, 356: 1175-1178. |
| [47] | Lumini E, Vallino M, Alguacil M M, Romani M, Bianciotto V. 2011. Different farming and water regimes in Italian rice fields affect arbuscular mycorrhizal fungal soil communities. Ecol Appl, 21(5): 1696-1707. |
| [48] | McMurdie P J, Holmes S. 2013. Phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8(4): e61217. |
| [49] | Miller M A, Pfeiffer W, Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop (GCE). November 14-14, 2010. New Orleans, LA, USA: IEEE: 1-8. |
| [50] | Oliver V, Cochrane N, Magnusson J, Brachi E, Monaco S, Volante A, Courtois B, Vale G, Price A, Teh Y A. 2019. Effects of water management and cultivar on carbon dynamics, plant productivity and biomass allocation in European rice systems. Sci Total Environ, 685: 1139-1151. |
| [51] | ?pik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij J M, Reier U, Zobel M. 2010. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol, 188(1): 223-241. |
| [52] | Parvin S, van Geel M, Yeasmin T, Lievens B, Honnay O. 2019. Variation in arbuscular mycorrhizal fungal communities associated with lowland rice (Oryza sativa) along a gradient of soil salinity and arsenic contamination in Bangladesh. Sci Total Environ, 686: 546-554. |
| [53] | Parvin S, van Geel M, Ali M M, Yeasmin T, Lievens B, Honnay O. 2021. A comparison of the arbuscular mycorrhizal fungal communities among Bangladeshi modern high yielding and traditional rice varieties. Plant Soil, 462(1): 109-124. |
| [54] | Price A H, Norton G J, Salt D E, Ebenhoeh O, Meharg A A, Meharg C, Islam M R, Sarma R N, Dasgupta T, Ismail A M, McNally K L, Zhang H, Dodd I C, Davies W J. 2013. Alternate wetting and drying irrigation for rice in Bangladesh: Is it sustainable and has plant breeding something to offer? Food Energy Secur, 2(2): 120-129. |
| [55] | R Core Team. 2021. R: A language and environment for statistical computing [2022-10-20]. https://www.R-project.org/. |
| [56] | Santos-Medellín C, Edwards J, Liechty Z, Nguyen B, Sundaresan V. 2017. Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes. mBio, 8(4): e00764-17. |
| [57] | Sarkodee-Addo E, Yasuda M, Gyu Lee C, Kanasugi M, Fujii Y, Ansong Omari R, Oppong Abebrese S, Bam R, Asuming- Brempong S, Mohammad Golam Dastogeer K, Okazaki S. 2020. Arbuscular mycorrhizal fungi associated with rice (Oryza sativa L.) in Ghana: Effect of regional locations and soil factors on diversity and community assembly. Agronomy, 10(4): 559. |
| [58] | Sawers R J H, Gutjahr C, Paszkowski U. 2008. Cereal mycorrhiza: An ancient symbiosis in modern agriculture. Trends Plant Sci, 13(2): 93-97. |
| [59] | Schreiner R P, Mihara K L. 2009. The diversity of arbuscular mycorrhizal fungi amplified from grapevine roots (Vitis vinifera L.) in Oregon vineyards is seasonally stable and influenced by soil and vine age. Mycologia, 101(5): 599-611. |
| [60] | Suzuki S, Kobae Y, Sisaphaithong T, Tomioka R, Takenaka C, Hata S. 2015. Differential growth responses of rice cultivars to an arbuscular mycorrhizal fungus, Funneliformis mosseae. J Hortic, 2(3): 142. |
| [61] | Tedersoo L, Sánchez-Ramírez S, K?ljalg U, Bahram M, D?ring M, Schigel D, May T, Ryberg M, Abarenkov K. 2018. High-level classification of the fungi and a tool for evolutionary ecological analyses. Fungal Divers, 90(1): 135-159. |
| [62] | Trouvelot A, Kough J L, Gianinazzi-Pearson V. 1986. Rate measurement of VA mycorrhization of a root system: Search for estimation methods with functional significance. In: Gianinazzi-Pearson V, Gianinazzi S. Mycorrhizae: Physiology and Genetics. Paris, France: INRA-Press: 217-221. |
| [63] | Vallino M, Greppi D, Novero M, Bonfante P, Lupotto E. 2009. Rice root colonisation by mycorrhizal and endophytic fungi in aerobic soil. Ann Appl Biol, 154(2): 195-204. |
| [64] | Vallino M, Fiorilli V, Bonfante P. 2014. Rice flooding negatively impacts root branching and arbuscular mycorrhizal colonization, but not fungal viability. Plant Cell Environ, 37(3): 557-572. |
| [65] | Wang Y T, Li T, Li Y W, Bj?rn L O, Rosendahl S, Olsson P A, Li S S, Fu X L. 2015. Community dynamics of arbuscular mycorrhizal fungi in high-input and intensively irrigated rice cultivation systems. Appl Environ Microbiol, 81(8): 2958-2965. |
| [66] | Wang Y T, Bao X Z, Li S S. 2021. Effects of arbuscular mycorrhizal fungi on rice growth under different flooding and shading regimes. Front Microbiol, 12: 756752. |
| [67] | Watanarojanaporn N, Boonkerd N, Tittabutr P, Longtonglang A, Teaumroong N. 2013. Effect of rice cultivation systems on indigenous arbuscular mycorrhizal fungal community structure. Microbes Environ, 28(3): 316-324. |
| [68] | White T J, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M A, Gelfand D H, Sninsky J J, White T J. PCR Protocols:A Guide to Methods and Applications. San Diego, USA: Academic Press: 315-322. |
| [69] | Wickham H, Averick M, Bryan J, Chang W, McGowan L, Fran?ois R, Grolemund G, Hayes A, Henry L, Hester J, Kuhn M, Pedersen T, Miller E, Bache S, Müller K, Ooms J, Robinson D, Seidel D, Spinu V, Takahashi K, Vaughan D, Wilke C, Woo K, Yutani H. 2019. Welcome to the tidyverse. J Open Source Softw, 4(43): 1686. |
| [70] | Wijayawardene N N, Hyde K D, Dai D Q, Sánchez-García M, Goto B T, Saxena R K, Erdo?du M, Sel?uk F, Rajeshkumar K C, Aptroot A, B?aszkowski J, Boonyuen N, da Silva G A, de Souza F A, Dong W, Ertz D, Haelewaters D, Jones E, Karunarathna S C, Kirk P M, Kukwa M, Kumla J, Leontyev D V, Lumbsch H T, Maharachchikumbura S, Marguno F, Martínez-Rodríguez P, Me?i? A, Monteiro J S, Oehl F, Paw?owska J, Pem D, Pfliegler W P, Phillips A, Po?ta A, He M Q, Li J X, Raza M, Sruthi O P, Suetrong S, Suwannarach N, Tedersoo L, Thiyagaraja V, Tibpromma S, Tkal?ec Z, Tokarev Y S, Wanasinghe D N, Wijesundara D, Wimalaseana S, Madrid H, Zhang G Q, Gao Y, Sánchez-Castro I, Tang L Z, Stadler M, Yurkov A, Thines M. 2022. Outline of fungi and fungus-like taxa: 2021. Mycosphere, 13(1): 53-453. |
| [71] | Xavier Martins W F, Rodrigues B F. 2020. Identification of dominant arbuscular mycorrhizal fungi in different rice ecosystems. Agric Res, 9(1): 46-55. |
| [72] | Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H. 2007. Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta, 225(4): 1031-1038. |
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