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Comparative RNA-Seq analysis of the root revealed transcriptional regulation system for aluminum tolerance in contrasting indica rice of North East India

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Abstract

Expression pattern of aluminum (Al) tolerance genes is one of the major determinants of Al avoidance/tolerance within plant cultivars. We have performed transcriptome analysis of two contrasting (Al-tolerant, Disang; Al-sensitive, Joymati) cultivars of India’s North Eastern region, an indica rice diversity hotspot, on exposure to excess Al3+ treatment in acidic condition. Co-expression analysis and SNPs enrichment analysis proposed the role of both trans-acting and cis-acting polymorphisms in Al signaling in the Al-tolerant cultivar. We proposed ten major genes, including arginine decarboxylase, phytase, and beta-glucosidase aggregating factor as candidates responsible for Al tolerance based on transcriptome analysis. Al3+ stress led to changes in the alternative splicing profile of the Al-tolerant cultivar. These studies demonstrated the transcriptional variations affiliated to Al avoidance/tolerance in contrasting indica rice of North East India and provided us with several candidate genes responsible for Al tolerance.

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Data availability

The datasets used and examined in the course of current study are available online in NCBI SRA database accession PRJNA675468 (https://www.ncbi.nlm.nih.gov/sra/PRJNA675468)

Abbreviations

Al:

Aluminum

SNPs:

Single nucleotide polymorphism

RNA-Seq:

mRNA sequencing

DR:

Disang rice

JR:

Joymati rice

FPKM:

Fragments per kilobase per million

IR:

Intron retention

AA:

Alternate 3′-acceptor

AD:

Alternate 5′-donor

ES:

Exon skip**

DEGs:

Differentially expressed genes

GO:

Gene ontology

SEA:

Singular enrichment analysis

ELP:

Expression level polymorphism

AS:

Alternative splicing

References

  • Aoki Y, Okamura Y, Tadaka S, Kinoshita K, Obayashi T (2015) ATTED-II in 2016: a plant coexpression database towards lineage-specific coexpression. Plant Cell Physiol 57:e5(1-9)

    Google Scholar 

  • Arenhart RA, Bai Y, de Oliveira LFV, Neto LB, Schunemann M, dos Santos Maraschin F et al (2014) New insights into aluminum tolerance in rice: the ASR5 protein binds the STAR1 promoter and other aluminum-responsive genes. Mol Plant 7(4):709–721

    Article  CAS  Google Scholar 

  • Awasthi JP, Saha B, Regon P, Sahoo S, Chowra U, Pradhan A, Roy A, Panda SK (2017) Morpho-physiological analysis of tolerance to aluminum toxicity in rice varieties of North East India. PLoS ONE 12(4):e0176357. https://doi.org/10.1371/journal.pone.0176357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Awasthi JP, Saha B, Panigrahi J, Yanase E, Koyama H, Panda SK (2019) Redox balance, metabolic fingerprint and physiological characterization in contrasting North East Indian rice for Aluminum stress tolerance. Sci Rep 9(1):1–21

    Article  Google Scholar 

  • Belgaroui N, Berthomieu P, Rouached H, Hanin M (2016) The secretion of the bacterial phytase PHY-US417 by Arabidopsis roots reveals its potential for increasing phosphate acquisition and biomass production during co-growth. Plant Biotechnol J 14:1914–1924

    Article  CAS  Google Scholar 

  • Conesa A, Madrigal P, Tarazona S, Gomez-Cabrero D, Cervera A, McPherson A, Szcześniak MW, Gaffney DJ, Elo LL, Zhang X, Mortazavi A (2016) A survey of best practices for RNA-seq data analysis. Genome Biol 17(1):13

    Article  Google Scholar 

  • Delker C, Quint M (2011) Expression level polymorphisms: heritable traits sha** natural variation. Trends Plant Sci 16:481–488

    CAS  PubMed  Google Scholar 

  • Devi SS, Saha B, Awasthi JP, Regon P, Panda SK (2020) Redox status and oxalate exudation determines the differential tolerance of two contrasting varieties of ‘Assam tea’ [Camelia sinensis (L.) O. Kuntz] in response to aluminum toxicity. Hortic Environ Biotechnol 61:485–499. https://doi.org/10.1007/s13580-020-00241-x

  • Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70

    Article  CAS  Google Scholar 

  • Egawa C, Kobayashi F, Ishibashi M, Nakamura T, Nakamura C, Takumi S (2006) Differential regulation of transcript accumulation and alternative splicing of a DREB2 homolog under abiotic stress conditions in common wheat. Genes Genet Syst 81:77–91

    Article  CAS  Google Scholar 

  • Famoso AN, Zhao K, Clark RT, Tung C-W, Wright MH, Bustamante C, Kochian LV, McCouch SR (2011) Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL map**. PLoS Genet 7:e1002221

    Article  CAS  Google Scholar 

  • Foissac S, Sammeth M (2015) Analysis of alternative splicing events in custom gene datasets by AStalavista. RNA Bioinforma 35:379–392

    Article  Google Scholar 

  • Guo P, Bai G, Carver B, Li R, Bernardo A, Baum M (2007) Transcriptional analysis between two wheat near-isogenic lines contrasting in aluminum tolerance under aluminum stress. Mol Gen Genomics 277:1–12

    Article  CAS  Google Scholar 

  • Guo C, Guo L, Li X, Ma C, Duan W, Gu J, Xu Z, Li R, Lu W, **ao K (2013) Transcriptional Regulation of the Rice Phytase Gene OsPHY1 by Several Phytohormones and Osmotic Stresses Using Promoter-GUS Analysis. Plant Mol Biol Report 31:1461–1473

    Article  CAS  Google Scholar 

  • Guo P, Qi Y-P, Yang L-T, Lai N-W, Ye X, Yang Y, Chen L-S (2017) Root adaptive responses to aluminum-treatment revealed by RNA-Seq in two citrus species with different aluminum-tolerance. Front Plant Sci 8:330

    PubMed  PubMed Central  Google Scholar 

  • Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann Bot 106:185–197

    Article  CAS  Google Scholar 

  • Houde M, Diallo AO (2008) Identification of genes and pathways associated with aluminum stress and tolerance using transcriptome profiling of wheat near-isogenic lines. BMC Genomics 9:400

    Article  Google Scholar 

  • Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21:655–667

    Article  CAS  Google Scholar 

  • Huang C-F, Yamaji N, Chen Z, Ma JF (2012) A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J 69:857–867

    Article  CAS  Google Scholar 

  • Iida K, Seki M, Sakurai T, Satou M, Akiyama K, Toyoda T, Konagaya A, Shinozaki K (2004) Genome-wide analysis of alternative pre-mRNA splicing in Arabidopsis thaliana based on full-length cDNA sequences. Nucleic Acids Res 32:5096–5103

    Article  CAS  Google Scholar 

  • Kauss H (1992) Callose and callose synthase. Mol Plant Pathol 2:1–8

    Google Scholar 

  • Kusunoki K, Nakano Y, Tanaka K, Sakata Y, Koyama H, Kobayashi Y (2017) Transcriptomic variation among six Arabidopsis thaliana accessions identified several novel genes controlling aluminium tolerance. Plant Cell Environ 40:249–263

    Article  CAS  Google Scholar 

  • Li J-Y, Liu J, Dong D, Jia X, McCouch SR, Kochian LV (2014) Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance. Proc Natl Acad Sci 111:6503–6508

    Article  CAS  Google Scholar 

  • Maejima E, Watanabe T, Osaki M, Wagatsuma T (2014) Phosphorus deficiency enhances aluminum tolerance of rice (Oryza sativa) by changing the physicochemical characteristics of root plasma membranes and cell walls. J Plant Physiol 171:9–15

    Article  CAS  Google Scholar 

  • Maron LG, Kirst M, Mao C, Milner MJ, Menossi M, Kochian LV (2008) Transcriptional profiling of aluminum toxicity and tolerance responses in maize roots. New Phytol 179:116–128

    Article  CAS  Google Scholar 

  • Nichol BE, Oliveira L a, Glass A, Siddiqi MY (1993) The effects of aluminum on the influx of calcium, potassium, ammonium, nitrate, and phosphate in an aluminum-sensitive cultivar of barley (Hordeum vulgare L.). Plant Physiol 101:1263–1266

    Article  CAS  Google Scholar 

  • Panda SK, Matsumoto H (2007) Molecular physiology of aluminum toxicity and tolerance in plants. Bot Rev 73:326–347

    Article  Google Scholar 

  • Panda SK, Baluška F, Matsumoto H (2009) Aluminum stress signaling in plants. Plant Signal Behav 4:592–597

    Article  CAS  Google Scholar 

  • Sagisaka S (1976) The occurrence of peroxide in a perennial plant Populas gelrica. Plant Physiol 57:308–309

    Article  CAS  Google Scholar 

  • Saha B, Swain D, Borgohain P, Rout GR, Koyama H, Panda SK (2020) Enhanced exudation of malate in the rhizosphere due to AtALMT1 overexpression in blackgram (Vigna mungo L.) confers increased aluminium tolerance. Plant Biol 22:701–708. https://doi.org/10.1111/plb.13112

  • Staiger D, Brown JWS (2013) Alternative splicing at the intersection of biological timing, development, and stress responses. Plant Cell 25:3640–3656

    Article  CAS  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    Article  CAS  Google Scholar 

  • **a J, Yamaji N, Kasai T, Ma JF (2010) Plasma membrane-localized transporter for aluminum in rice. Proc Natl Acad Sci 107:18381–18385

    Article  CAS  Google Scholar 

  • Yamaji N, Huang CF, Nagao S, Yano M, Sato Y, Nagamura Y, Ma JF (2009) A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21:3339–3349

    Article  CAS  Google Scholar 

  • Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinforma 13:134

    Article  CAS  Google Scholar 

  • Yokosho K, Yamaji N, Ma JF (2011) An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J 68:1061–1069

    Article  CAS  Google Scholar 

  • Yokosho K, Yamaji N, Fujii-Kashino M, Ma JF (2016) Functional analysis of a MATE gene OsFRDL2 revealed its involvement in Al-induced secretion of citrate, but a lower contribution to Al tolerance in rice. Plant Cell Physiol 57:976–985

    Article  CAS  Google Scholar 

  • Yu Y, ** C, Sun C, Wang J, Ye Y, Lu L, Lin X (2015) Elevation of arginine decarboxylase-dependent putrescine production enhances aluminum tolerance by decreasing aluminum retention in root cell walls of wheat. J Hazard Mater 299:280–288

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors sincerely thank the Regional Agricultural Research Station, Akbarpur (Karimganj), India, and Regional Rainfed Lowland Rice Research Station (RRLRRS) Gerua, Guwahati, Assam, India, for providing us with rice seeds. BS acknowledges the Science Education and Research Board (SERB) for National Post-Doctoral Fellowship (PDF/2018/003216).

Author information

Author notes

  1. Bedabrata Saha

    Present address: School of Biological Sciences, National Institute of Science Education and Research, Jatni, Odisha, 752050, India

  2. Sanjib Kumar Panda

    Present address: Department of Biochemistry, Central University of Rajasthan, Bandarsindri, Ajmer, 305817, India

  3. Jay Prakash Awasthi and Kazutaka Kusunoki contributed equally to this work.

Authors and Affiliations

  1. Plant Molecular Biotechnology Laboratory, Department of Life Science and Bioinformatics, Assam University, Silchar, Assam, 788011, India

    Jay Prakash Awasthi, Bedabrata Saha & Sanjib Kumar Panda

  2. Plant Cell Technology Laboratory, Faculty of Applied Biological Sciences, Gifu University, Gifu, 5011193, Japan

    Kazutaka Kusunoki, Yuriko Kobayashi & Hiroyuki Koyama

Authors
  1. Jay Prakash Awasthi
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  2. Kazutaka Kusunoki
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  3. Bedabrata Saha
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  4. Yuriko Kobayashi
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Contributions

S.K.P and H.K conceived and designed the study. J.P.A and B.S performed experimental works. K.K and Y.K performed RNA-Seq data processing, transcriptome analysis, and interpretation of the data. K.K, J.P.A, B.S, and S.K.P wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Sanjib Kumar Panda.

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Awasthi, J.P., Kusunoki, K., Saha, B. et al. Comparative RNA-Seq analysis of the root revealed transcriptional regulation system for aluminum tolerance in contrasting indica rice of North East India. Protoplasma 258, 517–528 (2021). https://doi.org/10.1007/s00709-020-01581-2

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