Phaseolus vulgaris MIR1511 genotypic variations differentially regulate plant tolerance to aluminum toxicity.


Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
03 2021
Historique:
revised: 20 11 2020
received: 24 06 2020
accepted: 03 12 2020
pubmed: 11 12 2020
medline: 7 8 2021
entrez: 10 12 2020
Statut: ppublish

Résumé

The common-bean (Phaseolus vulgaris), a widely consumed legume, originated in Mesoamerica and expanded to South America, resulting in the development of two geographically distinct gene pools. Poor soil condition, including metal toxicity, are often constraints to common-bean crop production. Several P. vulgaris miRNAs, including miR1511, respond to metal toxicity. The MIR1511 gene sequence from the two P. vulgaris model sequenced genotypes revealed that, as opposed to BAT93 (Mesoamerican), the G19833 (Andean) accession displays a 58-bp deletion, comprising the mature and star miR1511 sequences. Genotyping-By-Sequencing data analysis from 87 non-admixed Phaseolus genotypes, comprising different Phaseolus species and P. vulgaris populations, revealed that all the P. vulgaris Andean genotypes and part of the Mesoamerican (MW1) genotypes analyzed displayed a truncated MIR1511 gene. The geographic origin of genotypes with a complete versus truncated MIR1511 showed a distinct distribution. The P. vulgaris ALS3 (Aluminum Sensitive Protein 3) gene, known to be important for aluminum detoxification in several plants, was experimentally validated as the miR1511 target. Roots from BAT93 plants showed decreased miR1511 and increased ALS3 transcript levels at early stages under aluminum toxicity (AlT), while G19833 plants, lacking mature miR1511, showed higher and earlier ALS3 response. Root architecture analyses evidenced higher tolerance of G19833 plants to AlT. However, G19833 plants engineered for miR1511 overexpression showed lower ALS3 transcript level and increased sensitivity to AlT. Absence of miR1511 in Andean genotypes, resulting in a diminished ALS3 transcript degradation, appears to be an evolutionary advantage to high Al levels in soils with increased drought conditions.

Identifiants

pubmed: 33300202
doi: 10.1111/tpj.15129
doi:

Substances chimiques

MicroRNAs 0
RNA, Plant 0
Aluminum CPD4NFA903

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1521-1533

Informations de copyright

© 2020 Society for Experimental Biology and John Wiley & Sons Ltd.

Références

Aparicio-Fabre, R., Guillén, G., Loredo, M. et al. (2013) Common bean (Phaseolus vulgaris L.) PvTIFY orchestrates global changes in transcript profile response to jasmonate and phosphorus deficiency. BMC Plant Biol. 13, 26.
Arenas-Huertero, C., Pérez, B., Rabanal, F., Blanco-Melo, D., De la Rosa, C., Estrada-Navarrete, G., Sanchez, F., Covarrubias, A.A. and Reyes, J.L. (2009) Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol. Biol. 70, 385-401.
Ariani, A., BernyMieryTeran, J.C. and Gepts, P. (2018) Spatial and temporal scales of range expansion in wild Phaseolus vulgaris. Mol. Biol. Evol. 35, 119-131.
Axtell, M.J., Westholm, J.O. and Lai, E.C. (2011) Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol. 12, 221.
Beebe, S.E., Rao, I.M., Cajiao, C. and Grajales, M. (2008) Selection for drought resistance in common bean also improves yield in phosphorus limited and favorable environments. Crop Sci. 48, 582-592.
Berny Mier y Teran, J.C., Konzen, E.R., Medina, V., Palkovic, A., Ariani, A., Tsai, S.M., Gilbert, M.E. and Gepts, P. (2019a) Root and shoot variation in relation to potential intermittent drought adaptation of Mesoamerican wild common bean (Phaseolus vulgaris L.). Ann. Bot. 124, 917-932.
Berny Mier y Teran, J.C., Konzen, E.R., Palkovic, A., Tsai, S.M. and Gepts, P. (2020) Exploration of the yield potential of Mesoamerican wild common beans from contrasting eco-geographic regions by nested recombinant inbred populations. Front. Plant Sci. 11, 346.
Berny Mier y Teran, J.C., Konzen, E.R., Palkovic, A., Tsai, S.M., Rao, I.M., Beebe, S. and Gepts, P. (2019b) Effect of drought stress on the genetic architecture of photosynthate allocation and remobilization in pods of common bean (Phaseolus vulgaris L.), a key species for food security. BMC Plant Biol. 19, 171.
Bitocchi, E., Bellucci, E., Giardini, A. et al. (2013) Molecular analysis of the parallel domestication of the common bean (Phaseolus vulgaris) in Mesoamerica and the Andes. New Phytol. 197, 300-313.
Bitocchi, E., Nanni, L., Bellucci, E. et al. (2012) Mesoamerican origin of the common bean (Phaseolus vulgaris L.) is revealed by sequence data. Proc. Natl Acad. Sci. USA, 109, E788-E796.
Blair, M.W., López-Marín, H.D. and Rao, I.M. (2010) Identification of aluminum resistant Andean common bean (Phaseolus vulgaris L.) genotypes. Braz. J. Plant. Physiol. 21, 291-300.
Bojórquez-Quintal, E., Escalante-Magaña, C., Echevarría-Machado, I. and Martínez-Estévez, M. (2017) Aluminum, a friend or foe of higher plants in acid soils. Front. Plant Sci. 8(1767).
Broughton, W.J., Hernández, G., Blair, M., Beebe, S., Gepts, P. and Vanderleyden, J. (2003) Beans (Phaseolus spp.) - model food legumes. Plant Soil, 252, 55-128.
Chacón S, M.I., Pickersgill, B. and Debouck, D.G. (2005) Domestication patterns in common bean (Phaseolus vulgaris L.) and the origin of the Mesoamerican and Andean cultivated races. Theor. Appl. Genet. 110(3), 432-444. https://doi.org/10.1007/s00122-004-1842-2.
Chacón S, M.I., Pickersgill, B., Debouck, D.G. and Arias, J.S. (2007) Phylogeographic analysis of the chloroplast DNA variation in wild common bean (Phaseolus vulgaris L.) in the Americas. Plant Syst. Evol. 266(3-4), 175-195. https://doi.org/10.1007/s00606-007-0536-z
Dai, X., Zhuang, Z. and Zhao, P.X. (2018) psRNATarget: a plant small RNA target analysis server (2017 release). Nucleic Acids Res. 46, W49-W54.
Delgado-Salinas, A., Turley, T., Richman, A. and Lavin, M. (1999) Phylogenetic analysis of the cultivated and wild species of phaseolus (Fabaceae). Syst. Bot. 24, 438-460.
Ding, Y., Ding, L., Xia, Y., Wang, F. and Zhu, C. (2020) Emerging roles of microRNAs in plant heavy metal tolerance and homeostasis. J. Agric. Food Chem. 68, 1958-1965.
Dong, Z., Shi, L., Wang, Y., Chen, L., Cai, Z., Wang, Y., Jin, J. and Li, X. (2013) Identification and dynamic regulation of microRNAs involved in salt stress responses in functional soybean nodules by high-throughput sequencing. Int. J. Mol. Sci. 14, 2717-2738.
Dong, J., Piñeros, M.A., Li, X., Yang, H., Liu, Y., Murphy, A.S., Kochian, L.V. and Liu, D. (2017) An Arabidopsis ABC transporter mediates phosphate deficiency-induced remodeling of root architecture by modulating iron homeostasis in roots. Mol. Plant, 10, 244-259.
Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 113.
Estrada-Navarrete, G., Alvarado-Affantranger, X., Olivares, J.-E., Guillén, G., Díaz-Camino, C., Campos, F., Quinto, C., Gresshoff, P.M. and Sanchez, F. (2007) Fast, efficient and reproducible genetic transformation of Phaseolus spp. by Agrobacterium rhizogenes. Nat. Protoc. 2, 1819.
Eticha, D., Zahn, M., Bremer, M., Yang, Z., Rangel, A.F., Rao, I.M. and Horst, W.J. (2010) Transcriptomic analysis reveals differential gene expression in response to aluminium in common bean (Phaseolus vulgaris) genotypes. Ann. Bot. 105, 1119-1128.
Fahlgren, N., Howell, M.D., Kasschau, K.D., Chapman, E.J., Sullivan, C.M. and Cumbie, J.S. (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One, 2, e219.
Formey, D., Iñiguez, L.P., Peláez, P., Li, Y.-F., Sunkar, R., Sánchez, F., Reyes, J.L. and Hernández, G. (2015) Genome-wide identification of the Phaseolus vulgaris sRNAome using small RNA and degradome sequencing. BMC Genom. 16, 423.
Formey, D., Martín-Rodríguez, J.Á. and Hernández, G. (2019) Functional analysis of root microRNAs by a constitutive overexpression approach in a composite plant system. In Plant MicroRNAs (de Folter, S., ed). New York, NY: Springer, pp. 215-226.
Formey, D., Sallet, E., Lelandais-Briere, C., Ben, C.C., Bustos-Sanmamed, P. and Niebel, A. (2014) The small RNA diversity from Medicago truncatula roots under biotic interactions evidences the environmental plasticity of the miRNAome. Genome Biol. 15(457).
Franco, A.A. and Munns, D.N. (1982) Acidity and aluminum restraints on nodulation, nitrogen fixation, and growth of Phaseolus vulgaris in solution culture. Soil Sci. Soc. Am. J. 46, 296-301.
Frantzios, G., Galatis, B. and Apostolakos, P. (2001) Aluminium effects on microtubule organization in dividing root-tip cells of Triticum turgidum. Ii. Cytokinetic cells. J. Plant. Res. 114, 157-170.
Graham, P.H., Rosas, J.C., Estevez de Jensen, C., Peralta, E., Tlusty, B., Acosta-Gallegos, J. and Arraes Pereira, P.A. (2003) Addressing edaphic constraints to bean production: the Bean/Cowpea CRSP project in perspective. Field. Crop. Res. 82, 179-192.
Harris, I., Osborn, T.J., Jones, P. and Lister, D. (2020) Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Scientific Data, 7, 109.
Hoyos-Villegas, V., Song, Q. and Kelly, J.D. (2017) Genome-wide association analysis for drought tolerance and associated traits in common bean. Plant Genome, 10(1).
Htwe, N.M.P.S., Luo, Z.-Q., Jin, L.-G., Nadon, B., Wang, K.-J. and Qiu, L.-J. (2015) Functional marker development of miR1511-InDel and allelic diversity within the genus Glycine. BMC Genom. 16, 467.
Huang, R. and Li, W. (2011) Formation, distribution and risk control of landslides in China. J. Rock Mech. Geotech. Eng. 3, 97-116.
Huang, S.C., Lu, G.H., Tang, C.Y., Ji, Y.J., Tan, G.S., Hu, D.Q., Cheng, J., Wang, G.H., Qi, J.L. and Yang, Y.H. (2018) Identification and comparative analysis of aluminum-induced microRNAs conferring plant tolerance to aluminum stress in soybean. Biol. Plant. 62, 97-108.
Hwang, J.-U., Song, W.-Y., Hong, D. et al. (2016) Plant ABC transporters enable many unique aspects of a terrestrial plant's lifestyle. Mol. Plant, 9, 338-355.
IGBP-DIS-SoilData. (1998) A program for creating global soil-property databases, IGBP Global Soils Data Task. https://nelson.wisc.edu/sage/data-and-models/atlas/maps.php
Jones-Rhoades, M.W. and Bartel, D.P. (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell, 14(6), 787-799. https://doi.org/10.1016/j.molcel.2004.05.027
Katoh, K., Rozewicki, J. and Yamada, K.D. (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 20(4), 1160-1166.
Kami, J., Velasquez, V.B., Debouck, D.G. and Gepts, P. (1995) Identification of presumed ancestral DNA sequences of phaseolin in Phaseolus vulgaris. Proc. Nat. Acad. Sci. 92(4), 1101-1104. https://doi.org/10.1073/pnas.92.4.1101
Kim, J.W. and Minamikawa, T. (1996) Transformation and regeneration of French bean plants by the particle bombardment process. Plant Sci. 117, 131-138.
Klaedtke, S.M., Cajiao, C., Grajales, M., Polanía, J., Borrero, G., Guerrero, A., Rivera, M., Rao, I., Beebe, S.E. and Léon, J. (2012) Photosynthate remobilization capacity from drought-adapted common bean (Phaseolus vulgaris L.) lines can improve yield potential of interspecific populations within the secondary gene pool. J. Plant Breed. Crop Sci. 4, 49-61.
Klevebring, D., Street, N.R., Fahlgren, N., Kasschau, K.D., Carrington, J.C., Lundeberg, J. and Jansson, S. (2009) Genome-wide profiling of Populus small RNAs. BMC Genom. 10, 620.
Kochian, L.V., Hoekenga, O.A. and Piñeros, M.A. (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu. Rev. Plant Biol. 55, 459-493.
Koinange, E.M.K. and Gepts, P. (1992) Hybrid Weakness in Wild Phaseolus Vulgaris L. J. Hered. 83, 135-139.
Kumar, S., Stecher, G., Li, M., Knyaz, C. and Tamura, K. (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol. Biol. Evol. 35, 1547-1549.
Kwak, M. and Gepts, P. (2009) Structure of genetic diversity in the two major gene pools of common bean (Phaseolus vulgaris L., Fabaceae). Theor. Appl. Genet. 118, 979-992.
Larsen, P.B., Geisler, M.J.B., Jones, C.A., Williams, K.M. and Cancel, J.D. (2005) ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J. 41, 353-363.
Luo, Z., Jin, L. and Qiu, L. (2012) MiR1511 co-regulates with miR1511* to cleave the GmRPL4a gene in soybean. Chin. Sci. Bull. 57, 3804-3810.
Ma, J.F., Zheng, S.J., Matsumoto, H. and Hiradate, S. (1997) Detoxifying aluminium with buckwheat. Nature, 390, 569-570.
Mendoza-Soto, A.B., Naya, L., Leija, A. and Hernández, G. (2015) Responses of symbiotic nitrogen-fixing common bean to aluminum toxicity and delineation of nodule responsive microRNAs. Front. Plant Sci. 6(587).
Mukankusi, C., Raatz, B., Nkalubo, S., Berhanu, F., Binagwa, P., Kilango, M., Williams, M., Enid, K., Chirwa, R. and Beebe, S. (2019) Genomics, genetics and breeding of common bean in Africa: a review of tropical legume project. Plant Breed. 138, 401-414.
Mun, T., Bachmann, A., Gupta, V., Stougaard, J. and Andersen, S.U. (2016) Lotus Base: An integrated information portal for the model legume Lotus japonicus. Sci. Rep. 6, 39447.
Nozawa, M., Miura, S. and Nei, M. (2012) Origins and evolution of microRNA genes in plant species. Genome Biol. Evol. 4, 230-239.
Ossowski, S., Schwab, R. and Weigel, D. (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J. 53(4), 674-690. https://doi.org/10.1111/j.1365-313x.2007.03328.x
Peláez, P., Trejo, M.S., Iñiguez, L.P., Estrada-Navarrete, G., Covarrubias, A.A., Reyes, J.L. and Sanchez, F. (2012) Identification and characterization of microRNAs in Phaseolus vulgaris by high-throughput sequencing. BMC Genom. 13, 83.
Polania, J., Rao, I.M., Cajiao, C., Rivera, M., Raatz, B. and Beebe, S. (2016) Physiological traits associated with drought resistance in Andean and Mesoamerican genotypes of common bean (Phaseolus vulgaris L.). Euphytica, 210, 17-29.
Ramankutty, N., Foley, J.A., Norman, J. and McSweeney, K. (2002) The global distribution of cultivable lands: current patterns and sensitivity to possible climate change. Glob. Ecol. Biogeogr. 11, 377-392.
Rendón-Anaya, M., Herrera-Estrella, A., Gepts, P. and Delgado-Salinas, A. (2017a) A new species of Phaseolus (Leguminosae, Papilionoideae) sister to Phaseolus vulgaris, the common bean. Phytotaxa, 313(3), 259.
Rendón-Anaya, M., Montero-Vargas, J. M. and Saburido-Álvarez, S. (2017b) Genomic history of the origin and domestication of common bean unveils its closest sister species. Genome. Biol. 18(1), https://doi.org/10.1186/s13059-017-1190-6
Rogers, K. and Chen, X. (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell, 25, 2383.
Ruíz-Herrera, L.F. and López-Bucio, J. (2013) Aluminum induces low phosphate adaptive responses and modulates primary and lateral root growth by differentially affecting auxin signaling in Arabidopsis seedlings. Plant Soil, 371, 593-609.
Ryan, P.R., Tyerman, S.D., Sasaki, T., Furuichi, T., Yamamoto, Y., Zhang, W.H. and Delhaize, E. (2011) The identification of aluminium-resistance genes provides opportunities for enhancing crop production on acid soils. J. Exp. Bot. 62, 9-20.
Schier, G.A. and McQuattie, C.J. (2000) Effect of water stress on aluminum toxicity in pitch pine seedlings. J. Plant Nutr. 23, 637-647.
Schmutz, J., McClean, P.E., Mamidi, S. et al. (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat. Genet. 46, 707-713.
Song, X., Li, Y., Cao, X. and Qi, Y. (2019) MicroRNAs and their regulatory roles in plant-environment interactions. Annu. Rev. Plant Biol. 70, 489-525.
Šurbanovski, N., Brilli, M., Moser, M. and Si-Ammour, A. (2016) A highly specific microRNA-mediated mechanism silences LTR retrotransposons of strawberry. Plant J. 85, 70-82.
Valdés-López, O., Arenas-Huertero, C., Ramírez, M., Girard, L., Sánchez, F. and Vance, C.P. (2008) Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots. Plant Cell Environ. 31(12), 1834-1843.
Valdés-López, O., Yang, S.S., Aparicio-Fabre, R., Graham, P.H., Reyes, J.L. and Vance, C.P. (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol. 187, 805-818.
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome. Biol. 3(7), research0034.1. https://doi.org/10.1186/gb-2002-3-7-research0034
Vlasova, A., Capella-Gutiérrez, S., Rendón-Anaya, M. et al. (2016) Genome and transcriptome analysis of the Mesoamerican common bean and the role of gene duplications in establishing tissue and temporal specialization of genes. Genome Biol. 17, 32.
Wang, X., Wang, Z., Zheng, Z., Dong, J., Song, L., Sui, L., Nussaume, L., Desnos, T. and Liu, D. (2019) Genetic dissection of Fe-dependent signaling in root developmental responses to phosphate deficiency. Plant Physiol. 179, 300-316.
Xia, J., Yamaji, N., Kasai, T. and Ma, J.F. (2010) Plasma membrane-localized transporter for aluminum in rice. Proc. Natl Acad. Sci. USA, 107, 18381-18385.
Yang, Z.-B., Eticha, D., Albacete, A., Rao, I.M., Roitsch, T. and Horst, W.J. (2012) Physiological and molecular analysis of the interaction between aluminium toxicity and drought stress in common bean (Phaseolus vulgaris). J. Exp. Bot. 63, 3109-3125.
Zhang, Y., Guo, J., Chen, M., Li, L., Wang, L. and Huang, C.-F. (2018) The cell cycle checkpoint regulator atr is required for internal aluminum toxicity-mediated root growth inhibition in Arabidopsis. Front. Plant Sci. 9(118).

Auteurs

Jose Ángel Martín-Rodríguez (J)

Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Mexico.

Andrea Ariani (A)

Department of Plant Sciences, Section of Crop and Ecosystem Sciences, University of California, Davis, CA, USA.

Alfonso Leija (A)

Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Mexico.

Armando Elizondo (A)

Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Mexico.

Sara I Fuentes (SI)

Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Mexico.

Mario Ramirez (M)

Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Mexico.

Paul Gepts (P)

Department of Plant Sciences, Section of Crop and Ecosystem Sciences, University of California, Davis, CA, USA.

Georgina Hernández (G)

Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Mexico.

Damien Formey (D)

Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Mexico.

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