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Molybdenum (Mo) transporter genes in Panicoideae species: a genome-wide evolution study

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Abstract

Molybdenum (Mo) is one important mineral element for plants because it participates actively in many metabolic essential functions like the synthesis of molybdenum cofactor and nitrogen metabolism. Mo is available on soil in an anionic form, and its activity increases with pH elevation. Few studies in the literature reported the identification and characterization of Mo transporter genes. Given the above, we describe a comprehensive in silico analysis of Mo transporters in six Panicoideae species. We identified 15 candidates genes associated with Mo transporters. The subcellular location shows that all predicted genes were present in the plasma membrane. The genomic structure revealed that most of the Mo transporters genes showed no introns, while two sequences of P. virgatum presented one intron. Five conserved motifs and nine putative transmembrane domains were identified. Phylogenetic analysis revealed two groups (A1 and A2), showing close or conserved phylogenetic relationships. Synteny analysis identified 45 pairs of syntenic Mo orthologous among the six genomes of Panicoideae species, and purifying selection played a critical role in the evolution of Mo transporter genes. Efforts need to be undertaken to understand and improve molybdenum uptake and utilization in Panicoideae species for the sustainability of these species. This study will serve as a biotechnological basis for the characterization of candidate genes (Mo) involved in the regulation of gene expression under adverse conditions, allowing the development of future strategies to ensure greater sustainability of the important species of Panicoideae.

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Abbreviations

Mo:

Molybdenum

MOT1:

Molybdate transporter type 1

MOT2:

Molybdate transporter type 2

MW:

Molecular weight

pI:

Isoelectric point

TMDs:

Transmembrane domains

CDS:

Coding DNA sequence

NJ:

Neighbor-joining

SOX:

Sulfite oxidase aldehyde oxidase

NR:

Nitrate reductase

XO:

Xanthine oxidase

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  Google Scholar 

  • Arnon DI, Stout PR (1939) Molybdenum as an essential element for higher plants. Plant Physiol 14(3):599–602

    Article  CAS  Google Scholar 

  • Baxter I, Muthukumar B, Park HC, Buchner P, Lahner B et al (2008) Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1). PLoS Gene 4(2):e1000004

    Article  Google Scholar 

  • Bittner F (2014) Molybdenum metabolism in plants and crosstalk to iron. Front Plant Sci 5:28

    Article  Google Scholar 

  • Bohra A, Chand Jha U, Godwin ID, Varshney RK (2020) Genomic interventions for sustainable agriculture. Plant Biotechnol J 18:2388–2405

  • Compton EL, Karinou E, Naismith JH, Gabel F, Javelle A (2011) Low resolution structure of a bacterial SLC26 transporter reveals dimeric stoichiometry and mobile intracellular domains. J Biol Chem 286(30):27058–27067

    Article  CAS  Google Scholar 

  • de Leão RM, de Souza SGH, dos Santos TB (2020) An in silico mining of the ammonium transporter gene family in Ananas comosus L. Colloq Agrariae 16(6):10–24

    Article  Google Scholar 

  • dos Santos TB, Soares JDM, Lima JE, Silva JC, Ivamoto ST et al (2019) An integrated analysis of mRNA and sRNA transcriptional profiles in Coffea arabica L. roots: insights on nitrogen starvation responses. Funct Integr Genom 19(1):151–169

    Article  Google Scholar 

  • El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, Matloob Q, Richardson LJ, Salazar GA, Smart A, Sonnhammer ELL, Hirsh L, Paladin L, Piovesan D, Tosatto SCE, Finn RD (2018) The Pfam protein families database in 2019. Nucleic Acids Res 47(D1):D427–D432

    Article  Google Scholar 

  • Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. (2014) The Pfam protein families database. Nucleic Acids Res. 42:D222–30.

  • Gasber A, Klaumann S, Trentmann O, Trampczynska A, Clemens S et al (2011) Identification of an Arabidopsis solute carrier critical for intracellular transport and inter-organ allocation of molybdate. Plant Biol (stuttg) 13(5):710–718

    Article  CAS  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD et al (2012) Phytozome, a comparative platform for green plant genomics. Nucleic Acids Res 40:1178–1186

    Article  Google Scholar 

  • Guo C, Wang Y, Yang A, He J, Xiao C et al (2020) The Coix genome provides insights into panicoideae evolution and papery hull domestication. Mol Plant 13(2):309–320

    Article  CAS  Google Scholar 

  • Hippler FWR, Boaretto RM, Dovis VL, Gomes GOF, Quaggio JA, Quiñones A, Mattos-Jr D (2017) Revisiting nutrient management for Citrus production: to what extent does molybdenum affect nitrogen assimilation of trees? Sci Hort 225:462–470

    Article  CAS  Google Scholar 

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0, an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297

    Article  Google Scholar 

  • Huang XY, Liu H, Zhu YF, Pinson SRM, Lin HX, Guerinot ML, Zhao FJ, Salt DE (2019) Natural variation in a molybdate transporter controls grain molybdenum concentration in rice. New Phytol 221(4):1983–1997

    Article  CAS  Google Scholar 

  • Ide Y, Kusano M, Oikawa A, Fukushima A, Tomatsu H, Saito K, Hirai MY, Fujiwara T (2011) Effects of molybdenum deficiency and defects in molybdate transporter MOT1 on transcript accumulation and nitrogen/sulphur metabolism in Arabidopsis thaliana. J Exp Bot 62(4):1483–1497

    Article  CAS  Google Scholar 

  • Kellogg EA (2015) Viii. Subfamily panicoideae link (1827). In: Flowering plants. Monocots. The families and genera of vascular plants. Springer, Cham, Switzerland, pp 271–345

  • Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19(9):1639–1645

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 337:1870–1874

  • Li P, Luo T, Pu X, Zhou Y, Yu J, Liu L (2021) Plant transporters: roles in stress responses and effects on growth and development. Plant Growth Regul 93:253–266

    Article  CAS  Google Scholar 

  • Liu H, Xiong J, Jiang Y, Wang L, Cheng (Max) Z (2019) Evolution of the R2R3-MYB gene family in six Rosaceae species and expression in woodland strawberries. J Integr Agric 18(12):2753–2770

    Article  Google Scholar 

  • Morrell PL, Buckler ES, Ross-Ibarra J (2012) Crop genomics: advances and applications. Nat Rev Genet 13:85–96

    Article  CAS  Google Scholar 

  • Muthamilarasan M, Khandelwal R, Yadav CB, Bonthala VS, Khan Y, Prasad M (2014) Identification and molecular characterization of MYB transcription factor superfamily in C4 model plant Foxtail Millet (Setaria italica L.). PLoS ONE 9(10):e109920

    Article  Google Scholar 

  • Nie X, Zhao X, Wang S, Zhang T, Li C, Liu H, Tong W, Guo Y (2018) Complete chloroplast genome sequence of Broomcorn Millet (Panicum miliaceum L.) and comparative analysis with other Panicoideae species. Agronomy 8(9):159

    Article  CAS  Google Scholar 

  • Pandey S, Subramanaym RC, Yaqoob U, Negi YK, Arora S (2015) In silico analysis of cis acting regulatory elements CAREs in upstream regions of ascorbate glutathione pathway genes from Oryza sativa. Biochem Physiol 4(159):2

    Google Scholar 

  • Postel D, Vanlemmens P, Gode P, Ronco G, Villa P (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  Google Scholar 

  • Puranik S, Sahu PP, Mandal SN, B. VS, Parida SK, Prasad M. (2013) Comprehensive genome-wide survey, genomic constitution and expression profiling of the NAC transcription factor family in Foxtail Millet (Setaria italica L.). PLoS ONE 8(5):e64594

    Article  CAS  Google Scholar 

  • Qiao X, Li M, Li L, Yin H, Wu J, Zhang S (2015) Genome-wide identification and comparative analysis of the heat shock transcription factor family in Chinese white pear (Pyrus bretschneideri) and five other Rosaceae species. BMC Plant Biol 15:12

    Article  Google Scholar 

  • Rana M, Bhantana P, Sun X-C, Imran M, Shaaban M et al (2020) Molybdenum as an essential element for crops: an overview. Int J Sci Res Growth 24:18535

    Google Scholar 

  • Sharma A, Shahzad B, Kumar V, Kohli SK, Sidhu GPS, Bali AS, Kapoor D, Bhardwaj R, Zheng B (2019) Phytohormones regulate accumulation of osmolytes under abiotic stress. Biomolecules 9:285

    Article  CAS  Google Scholar 

  • Tejada-Jiménez M, Llamas Á, Sanz-Luque E, Galván A, Fernández E (2007) A high-affinity molybdate transporter in eukaryotes. Proc Natl Acad Sci USA 104(50):20126–20130

    Article  Google Scholar 

  • Tejada-Jiménez M, Gil-Díez P, León-Mediavilla J, Wen J, Mysore KS, Imperial J, González-Guerrero M (2017) Medicago truncatula Molybdate Transporter type 1 (MtMOT1.3) is a plasma membrane molybdenum transporter required for nitrogenase activity in root nodules under molybdenum deficiency. New Phytol 216(4):1223–1235

    Article  Google Scholar 

  • Tejada-Jimenez M, Chamiso-Ampudia A, Llamas A, Galvan A, Fernandez E (2018) Roles of molybdenum in plants and improvement of its acquisition and use efficiency. In: Hossain MA, Kamiya T, Burritt DJ, Phan Tran L-S, Fujiwara T (eds) Plant micronutrient use efficiency. Molecular and genomic perspectives in crop plants. Academic Press, Elsevier, Oxford, pp 137–159

    Google Scholar 

  • Tomatsu H, Takano J, Takahashi H, Watanabe-Takahashi A, Shibagaki N, Fujiwara T (2007) An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proc Natl Acad Sci USA 104(47):18807–18812

    Article  CAS  Google Scholar 

  • Vatansever R, Filiz E, Ozyigit II (2016) In silico identification and comparative analysis of molybdenum (Mo) transporter genes in plants. Braz J Bot 39:87–99

    Article  Google Scholar 

  • von Wittgenstein NJ, Le CH, Hawkins BJ, Ehlting J (2014) Evolutionary classification of ammonium, nitrate, and peptide transporters in land plants. BMC Evol Biol 14:11

    Article  Google Scholar 

  • Wang X, Cai X, Xu C, Wang Q (2021) Identification and characterization of the NPF, NRT2 and NRT3 in spinach. Plant Physiol Biochem 158:297–307

    Article  CAS  Google Scholar 

  • Wani SH, Kumar V, Shriram V, Sah SK (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4:162–176

    Article  Google Scholar 

  • Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins 64:643–651

    Article  CAS  Google Scholar 

  • Zhang Z, Li J, Zhao XQ, Wang J, Wong GKS, Yu J (2006) KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genom Proteom Bioinform 4:259–263

    Article  CAS  Google Scholar 

  • Zhang Y, Zalapa JE, Jakubowski AR, Price DL, Acharya A, Wei Y, Brummer EC, Kaeppler SM, Casler MD (2011) Post-glacial evolution of Panicum virgatum, centers of diversity and gene pools revealed by SSR markers and cpDNA sequences. Genetica 139:933–948

    Article  Google Scholar 

  • Zhao T, Schranz ME (2017) Network approaches for plant phylogenomic synteny analysis. Curr Opin Plant Biol 36:129–134

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil) (Grant: 2019/22642-0). Lorrayne Guimarães Bavaresco thanks to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES), finance code 001, for their research fellowship.

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Authors and Affiliations

  1. Postgraduate Program in Agronomy, Universidade do Oeste Paulista (UNOESTE), Presidente Prudente, SP, Brazil

    Lorrayne Guimarães Bavaresco, Alessandra Ferreira Ribas & Tiago Benedito dos Santos

  2. Agronomy Graduate Program, Universidade do Oeste Paulista (UNOESTE), Presidente Prudente, SP, Brazil

    Silviany Angelica Fernandes Silva

  3. Universidade Paranaense (UNIPAR), Umuarama, PR, Brasil

    Silvia Graciele Hülse de Souza

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  1. Lorrayne Guimarães Bavaresco
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  2. Silviany Angelica Fernandes Silva
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  4. Alessandra Ferreira Ribas
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  5. Tiago Benedito dos Santos
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Correspondence to Tiago Benedito dos Santos.

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Bavaresco, L.G., Silva, S.A.F., de Souza, S.G.H. et al. Molybdenum (Mo) transporter genes in Panicoideae species: a genome-wide evolution study. J. Crop Sci. Biotechnol. 25, 277–287 (2022). https://doi.org/10.1007/s12892-021-00130-4

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