Skip to main content
SpringerLink
Log in

Photosynthetic characterization and expression profiles of sugarcane infected by Sugarcane mosaic virus (SCMV)

  • Original article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Sugarcane mosaic virus (SCMV), belonging to genus Potyvirus, family Potyviridae, is a severe pathogen of several agricultural important crops, mainly sugarcane. Due to complex nature of sugarcane, the effect of SCMV pathogenicity on sugarcane photosynthetic systems remains to be explored. In this study, we investigated the alterations occurring in the photosynthetic system in the sugarcane genotypes at the cytopathological, physiological and biological, transcriptome and proteome level. We generated the transcriptome assembly of two genotypes (susceptible Badila and resistant B-48) using Saccharum spontaneum L. as a reference genome. RNA-sequencing data revealed the significant upregulation of NAD(P)H, RubisCO, oxygen-evolving complex, chlorophyll a and b binding protein, Psb protein family, PSI reaction center subunit II, and IVgenes in B-48, as compared to its counterparts. Upregulated genes in B-48 are associated with various processes such as stability and assembly of photosystem, protection against photoinhibition and antiviral defense. The expression pattern of differentially abundant genes were further verified at the proteomics level. Overall, differentially expressed genes/proteins (DEGs/DEPs) showed the consistency of expression at both transcriptome and proteome level in B-48 genotype. Comprehensively, these data supported the efficiency of B-48 genotype under virus infection conditions and provided a better understanding of the expression pattern of photosynthesis-related genes in sugarcane.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abbink TE, Peart JR, Mos TN, Baulcombe DC, Bol JF, Linthorst HJ (2002) Silencing of a gene encoding a protein component of the oxygen-evolving complex of photosystem II enhances virus replication in plants. Virology 295(2):307–319

    CAS  PubMed  Google Scholar 

  • Abel PP, Nelson RS, De B, Hoffmann N, Rogers SG, Fraley RT, Beachy RN (1986) Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232(4751):738–743

    CAS  PubMed  Google Scholar 

  • Akbar S, Tahir M, Wang M-B, Liu Q (2017) Expression analysis of hairpin RNA carrying Sugarcane mosaic virus (SCMV) derived sequences and transgenic resistance development in a model rice plant. BioMed Res Int. https://doi.org/10.1155/2017/1646140

    Article  PubMed  PubMed Central  Google Scholar 

  • Alexander MM, Cilia M (2016) A molecular tug-of-war: global plant proteome changes during viral infection. Curr Plant Biol 5:13–24

    Google Scholar 

  • Balachandran S, Osmond CB, Daley PF (1994) Diagnosis of the earliest strain-specific interactions between tobacco mosaic virus and chloroplasts of tobacco leaves in vivo by means of chlorophyll fluorescence imaging. Plant Physiol 104(3):1059–1065

    CAS  PubMed  PubMed Central  Google Scholar 

  • Balasubramaniam M, Kim B-S, Hutchens-Williams HM, Loesch-Fries LS (2014) The photosystem II oxygen-evolving complex protein PsbP interacts with the coat protein of Alfalfa mosaic virus and inhibits virus replication. Mol Plant Microbe Interact 27(10):1107–1118

    PubMed  Google Scholar 

  • Bhat S, Folimonova SY, Cole AB, Ballard KD, Lei Z, Watson BS, Sumner LW, Nelson RS (2013) Influence of host chloroplast proteins on Tobacco mosaic virus accumulation and intercellular movement. Plant Physiol 161(1):134–147

    CAS  PubMed  Google Scholar 

  • Bricker TM, Roose JL, Fagerlund RD, Frankel LK, Eaton-Rye JJ (2012) The extrinsic proteins of Photosystem II. Biochem Biophys Acta 1817:121–142

    CAS  PubMed  Google Scholar 

  • Caffarri S, Tibiletti T, Jennings RC, Santabarbara S (2014) A comparison between plant photosystem I and photosystem II architecture and functioning. Curr Protein Pept Sci 15(4):296–331. https://doi.org/10.2174/1389203715666140327102218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chu H-A, Chiu Y-F (2016) The roles of cytochrome b559 in assembly and photoprotection of Photosystem II revealed by site-directed mutagenesis studies. Front Plant Sci 6:1261

    PubMed  PubMed Central  Google Scholar 

  • Cousins AB, Baroli I, Badger MR, Ivakov A, Lea PJ, Leegood RC, von Caemmerer SJ (2007) The role of phosphoenolpyruvate carboxylase during C4 photosynthetic isotope exchange and stomatal conductance. Plant Physiol 145(3):1006–1017

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong M, Cheng G, Peng L, Xu Q, Yang Y, Xu J (2017) Transcriptome analysis of sugarcane response to the infection by Sugarcane steak mosaic virus (SCSMV). Tropical Plant Biol 10(1):45–55

    CAS  Google Scholar 

  • Dong-lin ZGHX (2005) On sugarcane viral diseases and their controlling. Acta Phytophylacica Sin 32(3):324–328

    Google Scholar 

  • Feki S, Loukili M, Triki-Marrakchi R, Karimova G, Old I, Ounouna H, Nato A, Nato F, Guesdon J-L, Lafaye P (2005) Interaction between tobacco Ribulose-l, 5-biphosphate Carboxylase/Oxygenase large subunit (RubisCO-LSU) and the PVY Coat Protein (PVY-CP). Eur J Plant Pathol 112(3):221–234

    CAS  Google Scholar 

  • Furbank RJPACT (2000) 9 C4 pathway.123

  • Geiger DR, Servaites JC (1994) Diurnal regulation of photosynthetic carbon metabolism in C3 plants. Annu Rev Plant Biol 45(1):235–256

    Google Scholar 

  • Geng C, Yan Z-Y, Cheng D-J, Liu J, Tian Y-P, Zhu C-X, Wang H-Y, Li X-D (2017) Tobacco vein banding mosaic virus 6K2 protein hijacks NbPsbO1 for virus replication. Sci Rep 7:43455

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gnanasekaran P, Ponnusamy K, Chakraborty S (2019) A geminivirus betasatellite encoded βC1 protein interacts with PsbP and subverts PsbP-mediated antiviral defence in plants. Mol Plant Pathol. https://doi.org/10.1111/mpp.12804

    Article  PubMed  PubMed Central  Google Scholar 

  • Gunasinghe U, Berger PH (1991) with chloroplasts in tobacco. Mol Plant Microbe Interact 4(5):452–457

    CAS  Google Scholar 

  • Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier C, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucl Acids Res 35(suppl_2):W585–W587

    PubMed  PubMed Central  Google Scholar 

  • Hunt S (2003) Measurements of photosynthesis and respiration in plants. Physiol Plant 117(3):314–325

    CAS  PubMed  Google Scholar 

  • Jang C, Seo E-Y, Nam J, Bae H, Gim YG, Kim HG, Cho IS, Lee Z-W, Bauchan GR, Hammond J (2013) Insights into Alternanthera mosaic virus TGB3 functions: interactions with Nicotiana benthamiana PsbO correlate with chloroplast vesiculation and veinal necrosis caused by TGB3 over-expression. Front Plant Sci 4:5

    PubMed  PubMed Central  Google Scholar 

  • Jensen PE, Bassi R, Boekema EJ, Dekker JP, Jansson S, Leister D, Robinson C, Scheller HV (2007) Structure, function and regulation of plant photosystem I. Biophys Acta 1767(5):335–352

    CAS  Google Scholar 

  • Jiménez I, López L, Alamillo J, Valli A, García JA (2006) Identification of a plum pox virus CI-interacting protein from chloroplast that has a negative effect in virus infection. Mol Plant Microbe Interact 19(3):350–358

    PubMed  Google Scholar 

  • Johnson MP (2016) Photosynthesis. Essays Biochem 60(3):255–273. https://doi.org/10.1042/EBC20160016

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M (2013) Data, information, knowledge and principle: back to metabolism in KEGG. Nucl Acids Res 42(D1):D199–D205

    PubMed  PubMed Central  Google Scholar 

  • Kong L, Wu J, Lu L, Xu Y, Zhou X (2014) Interaction between Rice stripe virus disease-specific protein and host PsbP enhances virus symptoms. Mol Plant 7(4):691–708

    CAS  PubMed  Google Scholar 

  • Kyseláková H, Prokopová J, Nauš J, Novák O, Navrátil M, Šafářová D, Špundová M, Ilík P (2011) Photosynthetic alterations of pea leaves infected systemically by pea enation mosaic virus: a coordinated decrease in efficiencies of CO2 assimilation and photosystem II photochemistry. Plant Physiol Biochem 49(11):1279–1289

    PubMed  Google Scholar 

  • Lakshmanan P, Geijskes RJ, Aitken KS, Grof CL, Bonnett GD, Smith GR (2005) Sugarcane biotechnology: the challenges and opportunities. In Vitro Cell Dev Biol 41(4):345–363

    CAS  Google Scholar 

  • Lehto K, Tikkanen M, Hiriart J-B, Paakkarinen V, Aro E-M (2003) Depletion of the photosystem II core complex in mature tobacco leaves infected by the flavum strain of tobacco mosaic virus. Mol Plant Microbe Interact 16(12):1135–1144

    CAS  PubMed  Google Scholar 

  • Ling H, Huang N, Wu Q, Su Y, Peng Q, Ahmed W, Gao S, Su W, Que Y, Xu L (2018) Transcriptional insights into the sugarcane-sorghum mosaic virus interaction. Tropical Plant Biol 11(3–4):163–176

    CAS  Google Scholar 

  • McQualter RB, Chong BF, Meyer K, Van Dyk DE, O'Shea MG, Walton NJ, Viitanen PV, Brumbley SM (2005) Initial evaluation of sugarcane as a production platform for p-hydroxybenzoic acid. Plant Biotechnol J 3(1):29–41

    CAS  PubMed  Google Scholar 

  • Newsholme SJ, Maleeft BF, Steiner S, Anderson NL, Schwartz LW (2000) Two-dimensional electrophoresis of liver proteins: characterization of a drug-induced hepatomegaly in rats. Electrophoresis 21:2122–2128

    CAS  PubMed  Google Scholar 

  • Otulak K, Chouda M, Bujarski J, Garbaczewska G (2015) The evidence of Tobacco rattle virus impact on host plant organelles ultrastructure. Micron 70:7–20

    CAS  PubMed  Google Scholar 

  • Putra LK, Kristini A, Achadian EM, Damayanti TA (2014) Sugarcane streak mosaic virus in Indonesia: distribution, characterisation, yield losses and management approaches. Sugar Tech 16(4):392–399

    CAS  Google Scholar 

  • Que Y, Xu L, Lin J, Ruan M, Zhang M, Chen R (2011) Differential protein expression in sugarcane during sugarcane-Sporisorium scitamineum interaction revealed by 2-DE and MALDI-TOF-TOF/MS. Comp Funct Genomics. https://doi.org/10.1155/2011/989016

    Article  PubMed  PubMed Central  Google Scholar 

  • Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33(suppl_2):W116–W120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raghavi S, Sindhu R, Binod P, Gnansounou E, Pandey A (2016) Development of a novel sequential pretreatment strategy for the production of bioethanol from sugarcane trash. Biores Technol 199:202–210

    CAS  Google Scholar 

  • Shi L-X, Lorković ZJ, Oelmüller R, Schröder WP (2000) The low molecular mass PsbW protein is involved in the stabilization of the dimeric photosystem II complex in Arabidopsis thaliana. J Biol Chem 275(48):37945–37950

    CAS  PubMed  Google Scholar 

  • Shukla D, Jilka J, Tosic M, Ford RE (1989) A novel approach to the serology of potyviruses involving affinity-purified polyclonal antibodies directed towards virus-specific N termini of coat proteins. J Gen Virol 70(1):13–23

    CAS  Google Scholar 

  • Singh P, Song Q-Q, Singh RK, Li H-B, Solanki MK, Yang L-T, Li Y-R (2019) Physiological and molecular analysis of sugarcane (Varieties—F134 and NCo310) during Sporisorium scitamineum interaction. Sugar Tech 21(4):631–644

    CAS  Google Scholar 

  • Stare T, Stare K, Weckwerth W, Wienkoop S, Gruden K (2017) Comparison between proteome and transcriptome response in potato (Solanum tuberosum L.) leaves following potato virus Y (PVY) infection. Proteomes 5(3):14

    PubMed Central  Google Scholar 

  • Su Y, Xu L, Wang Z, Peng Q, Yang Y, Chen Y, Que Y (2016) Comparative proteomics reveals that central metabolism changes are associated with resistance against Sporisorium scitamineum in sugarcane. BMC Genomics 17(1):800

    PubMed  PubMed Central  Google Scholar 

  • Użarowska A, Dionisio G, Sarholz B, Piepho H-P, Xu M, Ingvardsen CR, Wenzel G, Lübberstedt T (2009) Validation of candidate genes putatively associated with resistance to SCMV and MDMV in maize (Zea mays L.) by expression profiling. BMC Plant Biol 9(1):15

    PubMed  PubMed Central  Google Scholar 

  • Vogt L, Vinyard DJ, Khan S, Brudvig GW (2015) Oxygen-evolving complex of Photosystem II: an analysis of second-shell residues and hydrogen-bonding networks. Curr Opin Chem Biol 25:152–158

    CAS  PubMed  Google Scholar 

  • Wang Q, Zhang C, Wang C, Qian Y, Li Z, Hong J, Zhou X (2017) Further characterization of Maize chlorotic mottle virus and its synergistic interaction with Sugarcane mosaic virus in maize. Sci Rep 7:39960

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yao W, Ruan M, Qin L, Yang C, Chen R, Chen B, Zhang M (2017) Field performance of transgenic sugarcane lines resistant to sugarcane mosaic virus. Front Plant Sci 8:104

    PubMed  PubMed Central  Google Scholar 

  • Yu J, Knoppová J, Michoux F, Bialek W, Cota E, Shukla MK, Strašková A, Aznar GP, Sobotka R, Komenda J (2018) Ycf48 involved in the biogenesis of the oxygen-evolving photosystem II complex is a seven-bladed beta-propeller protein. Proc Natl Acad Sci 115(33):E7824–E7833

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zechmann B, Zellnig G (2009) Rapid diagnosis of plant virus diseases by transmission electron microscopy. J Virol Methods 162(1–2):163–169

    CAS  PubMed  Google Scholar 

  • Zhang M, Zhuo X, Wang J, Wu Y, Yao W, Chen R (2015) Effective selection and regeneration of transgenic sugarcane plants using positive selection system. In Vitro Cell Dev Biol 51(1):52–61

    CAS  Google Scholar 

  • Zhang M, Govindaraju MJST (2018) Sugarcane production in China. Sugarcane—technology and research. InTech, Rijeka. https://doi.org/10.5772/intechopen.73113

  • Zhang J, Zhang X, Tang H, Zhang Q, Hua X, Ma X, Zhu F, Jones T, Zhu X, Bowers J (2018a) Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat Genet 50(11):1565

    CAS  PubMed  Google Scholar 

  • Zulfugarov IS, Tovuu A, Eu Y-J, Dogsom B, Poudyal RS, Nath K, Hall M, Banerjee M, Yoon UC, Moon Y-H (2014) Production of superoxide from Photosystem II in a rice (Oryza sativa L.) mutant lacking PsbS. BMC Plant Biol 14(1):242

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We greatly appreciate Bioscience Editing Solutions for critically reading this paper and providing helpful suggestions.

Author information

Author notes

  1. Sehrish Akbar, Wei Yao, and Kai Yu have contributed equally to this paper.

Authors and Affiliations

  1. State Key Laboratory for Conservation and Utilization of Agro Bioresources, Guangxi University, Nanning, 530005, China

    Sehrish Akbar, Kai Yu, Lifang Qin, Miaohong Ruan, Baoshan Chen & Muqing Zhang

  2. Guangxi Key Laboratory for Sugarcane Biology, Guangxi University, Nanning, 530005, China

    Wei Yao

  3. IRREC-IFAS, University of Florida, Fort Pierce, FL, 34945, USA

    Charles A. Powell & Muqing Zhang

Authors
  1. Sehrish Akbar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kai Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lifang Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miaohong Ruan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Charles A. Powell
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Baoshan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Muqing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceived and designed the experiments: ZMQ and CBS. Performed the experiments: YW, RMH, QLF, SA and YK. Analyzed the data: RMH, YW, YK, SA, and ZMQ. Contributed reagents/materials/analysis tools: ZMQ and CBS. Wrote the paper: SA, YW, CP, and ZMQ. All authors read and approved the final version of the paper.

Corresponding author

Correspondence to Muqing Zhang.

Ethics declarations

Conflict of interest

The authors declared that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (RAR 1187 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akbar, S., Yao, W., Yu, K. et al. Photosynthetic characterization and expression profiles of sugarcane infected by Sugarcane mosaic virus (SCMV). Photosynth Res 150, 279–294 (2021). https://doi.org/10.1007/s11120-019-00706-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-019-00706-w

Keywords

Search

Navigation