Skip to main content
Log in

Expression quantitative trait loci analysis of the Rubisco activase gene in maize

  • Original Paper
  • Published:
Photosynthetica

Abstract

Expression quantitative trait loci (eQTL) analyses were applied in order to identify genetic factors that are relevant to the expression of a β-isoform Rubisco activase gene in maize, namely ZmRCAβ, in this study. During two years, a maize recombinant inbred line population was measured for ZmRCAβ expression levels at the grain filling stage. Based on a genetic map containing 916 molecular markers, we detected five eQTLs, namely qRCA2.1 on chromosome 2, and qRCA4.1, qRCA4.2, qRCA4.3, and qRCA4.4 on chromosome 4. These eQTLs explained the phenotypic variation ranging from 6.14% to 7.50% with the logarithm of the odd values ranging from 3.11 to 4.96. Based on the position of the eQTLs and ZmRCAβ on the chromosome, qRCA4.2 was inferred as a cis-eQTL and the remaining as a trans-eQTL, suggesting that a combination of both cis- and trans-acting elements might control ZmRCAβ expression. qRCA4.2, qRCA4.3, and qRCA4.4 were repeatedly detected during two years.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

eQTL:

expression quantitative trait loci

gDNA:

genomic DNA

LOD:

logarithm of the odd

RCA:

Rubisco activase

RIL:

recombinant inbred line

RuBP:

ribulose-1,5-bisphosphate

References

  • Ayala-Ochoa A., Vargas-Suárez M., Loza-Tavera H. et al.: In maize, two distinct ribulose 1,5-bisphosphate carboxylase/oxygenase activase transcripts have different day/night patterns of expression. — Biochimie 86: 439–449, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Chao M., Yin Z., Hao D. et al.: Variation in Rubisco activase (RCAβ) gene promoters and expression in soybean [Glycine max (L.) Merr.]. — J. Exp. Bot. 65: 47–59, 2014.

    Article  CAS  PubMed  Google Scholar 

  • DeRidder B.P., Shybut M.E., Dyle M.C. et al.: Changes at the 3´-untranslated region stabilize Rubisco activase transcript levels during heat stress in Arabidopsis. — Planta 236: 463–476, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Doss S., Schadt E.E., Drake T.A., Lusis A.J.: Cis-acting expression quantitative trait loci in mice. — Genome Res. 15: 681–691, 2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Druka A., Potokina E., Luo Z. et al.: Expression quantitative trait loci analysis in plants. — Plant Biotechnol. J. 8: 10–27, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Jansen R.C., Nap J.P.: Genetical genomics: the added value from segregation. — Trends Genet. 17: 388–391, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Kumar G.R., Sakthivel K., Sundaram R.M. et al.: Allele mining in crops: prospects and potentials. — Biotechnol. Adv. 28: 451–461, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Law R.D., Crafts-Brandner S.J.: High temperature stress increases the expression of wheat leaf ribulose-1,5-bisphosphate carboxylase/oxygenase activase protein. — Arch. Biochem. Biophys. 386: 261–267, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Li Q., Yang X., Bai G. et al.: Cloning and characterization of a putative GS3 ortholog involved in maize kernel development. — Theor. Appl. Genet. 120: 753–763, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Lorimer G.H.: The carboxylation and oxygenation of ribulose 1,5-bisphosphate: The primary events in photosynthesis and photorespiration. — Annu. Rev. Plant Physio. 32: 349–382, 1981.

    Article  CAS  Google Scholar 

  • Martínez-Barajas E., Molina-Galán J., Sánchez-de-Jiménez E.: Regulation of Rubisco activity during grain-fill in maize: possible role of Rubisco activase. — J. Agr. Sci. 128: 155–161, 1997.

    Article  Google Scholar 

  • Morales A., Ortega-Delgado M., Molina-Galán J., Sánchez-de-Jiménez E.S.: Importance of Rubisco activase in maize productivity based on mass selection procedure. — J. Exp. Bot. 50: 823–829, 1999.

    Article  CAS  Google Scholar 

  • Morley M., Molony C.M., Weber T.M. et al.: Genetic analysis of genome-wide variation in human gene expression. — Nature 430: 743–747, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murray M., Thompson W.F.: Rapid isolation of high molecular weight plant DNA. — Nucleic Acids Res. 8: 4321–4326, 1980.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parry M.A.J., Andralojc P.J., Mitchell R.A.C. et al.: Manipulation of Rubisco: the amount, activity, function and regulation. — J. Exp. Bot. 54: 1321–1333, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Portis A.R., Li C., Wang D., Salvucci M.E.: Regulation of Rubisco activase and its interaction with Rubisco. — J. Exp. Bot. 59: 1597–1604, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Portis A.R.: Rubisco activase–Rubisco's catalytic chaperone. — Photosynth. Res. 75: 11–27, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Qian J., Rodermel S.R.: Ribulose-1,5-bisphosphate carboxylase/oxygenase activase cDNAs from Nicotiana tabacum. — Plant Physiol. 102: 683–684, 1993.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rieseberg L.H., Archer M.A., Wayne R.K.: Transgressive segregation, adaptation and speciation. — Heredity 83: 363–372, 1999.

    Article  PubMed  Google Scholar 

  • Ristic Z., Momčilović I., Bukovnik U. et al.: Rubisco activase and wheat productivity under heat-stress conditions. — J. Exp. Bot. 60: 4003–4014, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Rundle S.J., Zielinski R.: Organization and expression of two tandemly oriented genes encoding ribulose-1,5-bisphosphate carboxylase/oxygenase activase in barley. — J. Biol. Chem. 266: 4677–4685, 1991.

    CAS  PubMed  Google Scholar 

  • Salvucci M.E., van de Loo F.J., Stecher D.: Two isoforms of Rubisco activase in cotton, the products of separate genes not alternative splicing. — Planta 216: 736–744, 2003.

    CAS  PubMed  Google Scholar 

  • Salvucci M.E., Werneke J.M., Ogren W.L., Portis A.R.: Purification and species distribution of Rubisco activase. — Plant Physiol. 84: 930–936, 1987.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schindler U., Menkens A.E., Beckmann H. et al.: Heterodimerization between light-regulated and ubiquitously expressed Arabidopsis GBF bZIP proteins. — Embo. J. 11: 1261–1273, 1992.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song H., Yin Z., Chao M. et al.: Functional properties and expression quantitative trait loci for phosphate transporter GmPT1 in soybean. — Plant Cell Environ. 37: 462–472, 2014.

    Article  CAS  PubMed  Google Scholar 

  • To K.Y., Suen D.F., Chen S.C.G.: Molecular characterization of ribulose-1,5-bisphosphate carboxylase/oxygenase activase in rice leaves. — Planta 209: 66–76, 1999.

    Article  CAS  PubMed  Google Scholar 

  • von Caemmerer S., Hendrickson L., Quinn V. et al.: Reductions of Rubisco activase by antisense RNA in the C4 plant Flaveria bidentis reduces Rubisco carbamylation and leaf photosynthesis. — Plant Physiol. 137: 747–755, 2005.

    Article  Google Scholar 

  • Wang G., Zhang J., Wang G. et al.: Proline responding plays a critical role in regulating general protein synthesis and the cell cycle in maize. — Plant Cell 26: 2582–2600, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S., Basten C., Zeng Z.: Windows QTL Cartographer V2. 5. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm. 2006.

    Google Scholar 

  • Werneke J.M., Chatfield J.M., Ogren W.L.: Alternative mRNA splicing generates the two ribulose-1,5-bisphosphate carboxylase/ oxygenase activase polypeptides in spinach and Arabidopsis. — Plant Cell 1: 815–825, 1989.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Werneke J.M., Zielinski R.E., Ogren W.L.: Structure and expression of spinach leaf cDNA encoding ribulose-1,5-bisphosphate carboxylase/oxygenase activase. — P. Natl. Acad. Sci. USA 85: 787–791, 1988.

    Article  CAS  Google Scholar 

  • Wu H., Li L., Jing Y., Kuang T.: Over-and anti-sense expressions of the large isoform of ribulose-1,5-bisphosphate carboxylase/oxygenase activase gene in Oryza sativa affect the photosynthetic capacity. — Photosynthetica 45: 194–201, 2007.

    Article  CAS  Google Scholar 

  • Xu Y.: Quantitative trait loci, separating, pyramiding, and cloning. — In: Janick J. (ed.): Plant Breeding Reviews, Vol. 15. Pp. 85–139, John Wiley & Sons, New York 1997.

    Google Scholar 

  • Yamori W., Masumoto C., Fukayama H. Makino A.: Rubisco activase is a key regulator of non-steady-state photosynthesis at any leaf temperature and, to a lesser extent, of steady-state photosynthesis at high temperature. — Plant J. 71: 871–880, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Yang Z., Lu Q., Wen X. et al.: Functional analysis of the rice rubisco activase promoter in transgenic Arabidopsis. — Biochem. Bioph. Res. Co. 418: 565–570, 2012.

    Article  CAS  Google Scholar 

  • Yin Z., Meng F., Song H. et al.: GmFtsH9 expression correlates with in vivo photosystem II function: chlorophyll a fluorescence transient analysis and eQTL mapping in soybean. — Planta 234: 815–827, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Yin Z., Meng F., Song H. et al.: Expression quantitative trait loci analysis of two genes encoding rubisco activase in soybean. — Plant Physiol. 152: 1625–1637, 2010

    Article  CAS  PubMed  Google Scholar 

  • Yin Z., Qin Q., Wu F. et al.: Quantitative trait locus mapping of chlorophyll a fluorescence parameters using a recombinant inbred line population in maize. — Euphytica 205: 25–35, 2015.

    Article  CAS  Google Scholar 

  • Yin Z., Wang Y., Wu F. et al.: Quantitative trait locus mapping of resistance to Aspergillus flavus infection using a recombinant inbred line population in maize. — Mol. Breeding 33: 39–49, 2014a.

    Article  CAS  Google Scholar 

  • Yin Z., Zhang Z., Deng D. et al.: Characterization of Rubisco activase genes in maize: an α-isoform gene functions alongside a β-isoform gene. — Plant Physiol. 164: 2096–2106, 2014b.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H., Hao D., Sitoe H.M. et al.: Genetic dissection of the relationship between plant architecture and yield component traits in soybean (Glycine max) by association analysis across multiple environments. — Plant Breeding 134: 564–572, 2015.

    Article  Google Scholar 

  • Zhang N., Portis A.R.: Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. — P. Natl. Acad. Sci. USA 96: 9438–9443, 1999.

    Article  CAS  Google Scholar 

  • Zhao K., Tung C.W., Eizenga G.C. et al.: Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. — Nat. Commun. 2: 467, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zuo W., Chao Q., Zhang N. et al.: A maize wall-associated kinase confers quantitative resistance to head smut. — Nat. Genet. 47: 151–157, 2015.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Z. T. Yin.

Additional information

Acknowledgments: This work received grant support in part from the National Natural Science Foundation of China (31571669, 91535106), the Jiangsu Natural Science Fund (BK20141272), the Agricultural Branch of the Technology Supported Program of Jiangsu Province (BE2014353, BE2013434), the Jiangsu Agriculture Science and Technology Innovation Fund (CX(14)5087), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, Q., Zhang, Y., Chen, B. et al. Expression quantitative trait loci analysis of the Rubisco activase gene in maize. Photosynthetica 55, 329–337 (2017). https://doi.org/10.1007/s11099-016-0242-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-016-0242-6

Additional key words

Navigation