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Towards efficient photosynthesis: overexpression of Zea mays phosphoenolpyruvate carboxylase in Arabidopsis thaliana

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Abstract

Plants with C4 photosynthesis are efficient in carbon assimilation and have an advantage over C3 photosynthesis. In C4 photosynthesis, the primary CO2 fixation is catalyzed by phosphoenolpyruvate carboxylase (PEPC). Here, we show that overexpression of Zea mays PEPC cDNA, under the control of 35S promoter, in Arabidopsis thaliana resulted in ~7–10 fold higher protein abundance and ~7–10 fold increase in PEPC activity in the transgenic lines than that in the vector control. We suggest that overexpression of PEPC played an anaplerotic role to increase the supply of 4-carbon carboxylic acids, which provided carbon skeletons for increased amino acid and protein synthesis. Higher protein content must have been responsible for increased metabolic processes including chlorophyll biosynthesis, photosynthesis, and respiration. Consequently, the PEPC-overexpressed transgenic plants had higher chlorophyll content, enhanced electron transport rate (ETR), lower non-photochemical quenching (NPQ) of chlorophyll a fluorescence, and a higher performance index (PI) than the vector control. Consistent with these observations, the rate of CO2 assimilation, the starch content, and the dry weight of PEPC-overexpressed plants increased by 14–18 %, 10–18 %, and 6.5–16 %, respectively. Significantly, transgenics were tolerant to salt stress as they had increased ability to synthesize amino acids, including the osmolyte proline. NaCl (150 mM)-treated transgenic plants had higher variable to maximum Chl a fluorescence (F v/F m) ratio, higher PI, higher ETR, and lower NPQ than the salt-treated vector controls. These results suggest that expression of C4 photosynthesis enzyme(s) in a C3 plant can improve its photosynthetic capacity with enhanced tolerance to salinity stress.

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Abbreviations

APT:

Adenine phosphoribosyl transferase

CaMV:

Cauliflower mosaic virus

Chl:

Chlorophyll

EDTA:

Ethylenediaminetetraacetic acid

ETR:

Electron transport rate, see text for details

F m :

Maximum Chl fluorescence

F o :

Minimum Chl fluorescence

F v :

Variable fluorescence, F m − F o

gs:

Stomatal conductance

LED:

Light-emitting diode

MDA:

Malondialdehyde, CH2(CHO)2

MDH:

Malate dehydrogenase

ME:

Malic enzyme

MS:

Murashige and Skoog medium

NPQ:

Non-photochemical quenching (of Chl fluorescence)

nptII:

Neomycin phosphotransferase (kanamycin resistance gene)

OAA:

Oxaloacetic acid

PAR:

Photosynthetically active radiation

PEP:

Phosphoenolpyruvate

PEPC:

Phosphoenolpyruvate carboxylase

PFD:

Photon flux density

PI:

Performance index, see text for details

PMSF:

Phenylmethylsulfonyl fluoride

PSI:

Photosystem I

PSII:

Photosystem II

PVP:

Polyvinylpyrrolidone

qE:

Energy-dependent quenching of the excited state of Chl a

qI:

Photoinhibitory quenching of the excited state of Chl a

qT:

State transition quenching of the excited state of Chl a

RC/ABS:

Density of reaction centers per PSII antenna chlorophyll (see text for details)

RC:

Reaction center

ROS:

Reactive oxygen species

RuBisCO:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

TAE:

Tris-base, acetic acid and EDTA

TEM:

Transmission electron microscopy

VC:

Vector control

WT:

Wild type

WUE:

Water use efficiency

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Acknowledgments

We thank Professor A.S. Raghavendra of the University of Hyderabad for providing us the anti-maize PEPC antibody. We also thank Kamal Ruhil and Barnali Padhi for their generous help in the experiments presented here. This work was supported by the National Agriculture Innovation Project (Grant No. NAIP/C4/C2043/2008-09 to BCT), from the Indian Council Agriculture Research, and Sir Jagdish Chandra Bose Fellowship to BCT. Govindjee thanks JNU for Visiting Professorship in its School of Life Sciences, and GIAN (Global Initiative on Academic Network, Ministry of Human Resources, Govt. of India) to lecture in the Spring of 2016 at JNU; he also thanks Rayme Dorsey (Plant Biology) for helping him with office work, and Jeff Haas and all the staff at Information Technology, Life Sciences, University of Illinois at Urbana-Champaign for helping him with both software and hardware related to the use of computers.

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Authors and Affiliations

  1. School of Life Sciences, Jawaharlal Nehru University, New Delhi, 110067, India

    Deepika Kandoi & Baishnab C. Tripathy

  2. School of Biotechnology, Kalinga Institute of Industrial Technology University, Bhubaneswar, Odisha, 751024, India

    Deepika Kandoi & Sasmita Mohanty

  3. Department of Plant Biology, Department of Biochemistry and Center of Biophysics & Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Govindjee

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  1. Deepika Kandoi
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  2. Sasmita Mohanty
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  3. Govindjee
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  4. Baishnab C. Tripathy
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Correspondence to Baishnab C. Tripathy.

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The authors honor George C. Papageourgiou, who was a good friend of Late Prasanna Mohanty, B. C. Tripathy’s mentor; both Papageorgiou and Mohanty were Ph.D. students of one of us (Govindjee).

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Kandoi, D., Mohanty, S., Govindjee et al. Towards efficient photosynthesis: overexpression of Zea mays phosphoenolpyruvate carboxylase in Arabidopsis thaliana . Photosynth Res 130, 47–72 (2016). https://doi.org/10.1007/s11120-016-0224-3

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