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The expression of cyanobacterial glycolate–decarboxylation pathway genes improves biomass accumulation in Arabidopsis thaliana

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Abstract

Transgenic Arabidopsis thaliana plants expressing cyanobacterial decarboxylation genes GLCD1 (GLYCOLATE DEHYDROGENASE I), HDH (HYDROXYACID DEHYDROGENASE), ODC (OXALATE DECARBOXYLASE) alone, and HDH::ODC simultaneously were successfully developed. Plants independently expressing GLCD1, HDH, ODC, and HDH::ODC were referred to as GD, HD, OX, and HX plants, respectively. The single-copy homozygous GD, HD, OX, and HX plants exhibited appreciable expression of chimeric genes. Phenotypic characterization demonstrated that rosette diameter of GD, HD, OX, and HX was 20, 22, 17, and 16% higher than wild-type (WT) plants. Total numbers of leaves were 32, 35, 37, and 34% more than WT plants after 32 days of sowing. Similarly, all transgenic plants produced more cauline branches than WT plants. All transgenic plants gained more height as compared to WT when recorded after 42 days of growth except HX transgenic plants. Plants vegetative dry biomass was 43% (GD), 35% (HD), 42% (OX), and 36% (HX) higher than WT plants. This is the first report on characterization of cyanobacterial decarboxylation pathway genes, which will pave the way for transformation of complete pathway in plants for better biomass accumulation.

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References

  • Agarie S, Miura A, Sumikura R, Tsukamoto S, Nose A, Arima S, Matsuoka M, Miyao-Tokutomi M (2002) Overexpression of C4 PEPC caused O2-insensitive photosynthesis in transgenic rice plants. Plant Sci 162:257–265

    Article  CAS  Google Scholar 

  • Ahmad R, Bilal M, Jeon JH, Soon KH, Park YI, Shah M, Kwon SY (2016) Improvement of biomass accumulation of potato plants by transformation of cyanobacterial photorespiratory glycolate catabolism pathway genes. Plant Biotechnol Rep 10:269–276

    Article  Google Scholar 

  • Andrews JT, Whitney SM (2003) Manipulating ribulose bisphosphate carboxylase/oxygenase in the chloroplasts of higher plants. Arch Biochem Biophys 414:159–169

    Article  CAS  Google Scholar 

  • Campbell WJ, Ogren WL (1990) Glyoxylate inhibition of Ribulosebiphosphate carboxylase-oxygenase: activation in intact, lysed and reconstituted chloroplasts. Photosynth Res 23:257–268

    Article  CAS  PubMed  Google Scholar 

  • Clough S, Bent A (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Dalal J, Lopez H, Vasani NB, Hu Z, Swift JE, Yalamanchill R, Dvora M, Lin X, Qu R, Sederoff HW (2015) A photorespiratory bypass increases plant growth and seed yield in biofuel crop Camelina sativa. Biotechnol Biofuels 8:175–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawe D (2007) Agricultural research, poverty alleviation and key trends in Asia’s rice economy. In: Sheehy JE, Mitchell PL, Hardy B (eds) Charting new pathways to C4 rice. World Scientific Publishing Co. Pte. Ltd., Singapore, pp 37–55

    Google Scholar 

  • Eisenhut M, Wolfgang R, Maya H, Hermann B, Aaron K, Martin H (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. PNAS 105(44):17199–17204

    Article  PubMed  Google Scholar 

  • Engqvist M, Drincovich MF, Flugge UI, Maurino VG (2009) Two D-2-hydroxy-acid dehydrogenases in Arabidopsis thalina with catalytic capacities to participate in the last reaction of the methylglyoxal and β-oxidation pathways. J Biol Chem 284(37):25026–25037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch HJ, Rosenkranz R, St€abler N, Sch€onfeld B, Kreuzaler F, Peterhansel C (2007) Chloroplast photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat Biotechnol 25:593–599

    Article  CAS  PubMed  Google Scholar 

  • Ku SB, Kano MY, Matsuoka M (1996) Evolution and expression of C4 photosynthesis genes. Plant Physiol 111:949–957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Ren B, Ding L, Shen Q, Peng S, Guo S (2013) Does chloroplast size influence photosynthetic nitrogen use efficiency? PLoS One 8(4):e62036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maier A, Fahnenstich H, Von Caemmerer S, Engqvist MK, Weber APM, Flugge UI, Maurino VG (2012) Glycolate oxidation in A. thaliana chloroplasts improves biomass production. Front Plant Sci 3:38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nölke G, Houdelet M, Kreuzaler F, Peterhansal C, Schillberg S (2014) The expression of a recombinant glycolate dehydrogenase polyprotein in potato (Solanum tuberosum) plastids strongly enhances photosynthesis and tuber yield. Plant Biotechnol J 12:734–742

    Article  CAS  PubMed  Google Scholar 

  • Oliver DJ (1978) Effect of glyoxylate on sensitivity of net photosynthesis to oxygen (the warburg effect) in tobacco. Plant Physiol 62:938–940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peterhansel C, Maurino VG (2011) Photorespiration redesigned. Plant Physiol 155:49–55

    Article  CAS  PubMed  Google Scholar 

  • Raines CA, Paul MJ (2006) Products of leaf primary carbon metabolism modulate the developmental programme determining plant morphology. J Exp Bot 57:1857–1862

    Article  CAS  PubMed  Google Scholar 

  • Somerville CR (2001) An early Arabidopsis demonstration. Resolving a few issues concerning photorespiration. Plant Physiol 125:20–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • South PF, Cavanagh AP, Lopez-Calcago PE, Raines CA, Ort DR (2018) Optimising photorespiration for improved productivity. J Integr Plant Biol 60(12):1217–1230

    Article  CAS  PubMed  Google Scholar 

  • Timm S, Wittmiß M, Gamlien S, Ewald R, Florian A, Frank M, Wirtz M, Hell R, Fernie AR, Bauwe H (2015) Mitochondrial dihydrolipoyl dehydrogenase activity shapes photosynthesis and photorespiration of Arabidopsis thaliana. Plant Cell 27:1968–1984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Von C, Furbank RT (2003) The C4 pathway: an efficient CO2 pump. Photosynth Res 77:191–207

    Article  Google Scholar 

  • Wang F, Chen X, Zhang F, Niu Y, Ye Y, Qi S, Zhou Q (2017) A soybean plastidic ATD/ADP transporter gene, GmAATP, is involved in carbohydrate metabolism in transgenic Arabidopsis. Plant Biotechnol Rep 11:135–146

    Article  Google Scholar 

  • Wu J, Zhang Z, Zhang Q, Han X, Gu X, Lu T (2015) The molecular cloning and clarification of a photorespiratory mutant, oscdm1, using enhancer trapping. Front Genet 6:1–17

    Google Scholar 

  • Zhu XG, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Trends Biotechnol 19:153–159

    CAS  Google Scholar 

  • Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61(1):235–261

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Higher Education Commission of Pakistan for IRSIP funding to Misbah Bilal and funding via HEC-NRPU project no. 20-4301/RD/HEC/14/619 to conduct the study.

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Correspondence to Bruce Osborne or Raza Ahmad.

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Bilal, M., Abbasi, A.Z., Khurshid, G. et al. The expression of cyanobacterial glycolate–decarboxylation pathway genes improves biomass accumulation in Arabidopsis thaliana. Plant Biotechnol Rep 13, 361–373 (2019). https://doi.org/10.1007/s11816-019-00548-x

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