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Photosynthetic antenna engineering to improve crop yields

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Abstract

Main conclusion

Evidence shows that decreasing the light-harvesting antenna size of the photosystems in tobacco helps to increase the photosynthetic productivity and plant canopy biomass accumulation under high-density cultivation conditions.

Decreasing, or truncating, the chlorophyll antenna size of the photosystems can theoretically improve photosynthetic solar energy conversion efficiency and productivity in mass cultures of algae or plants by up to threefold. A Truncated Light-harvesting chlorophyll Antenna size (TLA), in all classes of photosynthetic organisms, would help to alleviate excess absorption of sunlight and the ensuing wasteful non-photochemical dissipation of excitation energy. Thus, solar-to-biomass energy conversion efficiency and photosynthetic productivity in high-density cultures can be increased. Applicability of the TLA concept was previously shown in green microalgae and cyanobacteria, but it has not yet been demonstrated in crop plants. In this work, the TLA concept was applied in high-density tobacco canopies. The work showed a 25% improvement in stem and leaf biomass accumulation for the TLA tobacco canopies over that measured with their wild-type counterparts grown under the same ambient conditions. Distinct canopy appearance differences are described between the TLA and wild type tobacco plants. Findings are discussed in terms of concept application to crop plants, leading to significant improvements in agronomy, agricultural productivity, and application of photosynthesis for the generation of commodity products in crop leaves.

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Abbreviations

Car:

Carotenoids

PS:

Photosystem

TLA:

Truncated light-harvesting antenna

References

  • Abadia J, Glick RE, Taylor SE, Terry N, Melis A (1985) Photochemical apparatus organization in the chloroplasts of two Beta vulgaris genotypes. Plant Physiol 79:872–878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alexandratos N, Bruinsma J (2012) World Agriculture: Towards 2030/2050. The 2012 revision. ESA Working Paper No. 12-03, Food Agric Org, Rome

  • Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annu Rev Plant Physiol 37:93–136

    Article  CAS  Google Scholar 

  • Andrianov V, Borisjuk N, Pogrebnyak N et al (2010) Tobacco as a production platform for biofuel: overexpression of Arabidopsis DGAT and LEC2 genes increases accumulation and shifts the composition of lipids in green biomass. Plant Biotechnol J 8:277–287

    Article  CAS  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cazzaniga S, Dall’Osto L, Szaub J, Scibilia L, Ballottari M, Purton S, Bassi R (2014) Domestication of the green alga Chlorella sorokiniana: reduction of antenna size improves light-use efficiency in a photobioreactor. Biotechnol Biofuels 7(1):157

    Article  PubMed  PubMed Central  Google Scholar 

  • De Mooij T, Janssen M, Cerezo-Chinarro O et al (2015) Antenna size reduction as a strategy to increase biomass productivity: a great potential not yet realized. J Appl Phycol 27:1063–1077

    Article  Google Scholar 

  • Fitzmaurice WP, Nguyen LV, Wernsman EA, Thompson WF, Conkling MA (1999) Transposon tagging of the sulfur gene of tobacco using engineered maize ac/ds elements. Genetics 153:1919–1928

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghirardi ML, Melis A (1988) Chlorophyll b-deficiency in soybean mutants. I. Effects on photosystem stoichiometry and chlorophyll antenna size. Biochim Biophys Acta 932:130–137

    Article  CAS  Google Scholar 

  • Ghirardi ML, McCauley SW, Melis A (1986) Photochemical apparatus organization in the thylakoid membrane of Hordeum vulgare wild type and chlorophyll b-less chlorina f2 mutant. Biochim Biophys Acta 851:331–339

    Article  CAS  Google Scholar 

  • Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Camilla Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818

    Article  CAS  PubMed  Google Scholar 

  • Greene BA, Staehelin LA, Melis A (1988) Compensatory alterations in the photochemical apparatus of a photoregulatory, chlorophyll b-deficient mutant of maize. Plant Physiol 87:365–370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hansson A, Gamini Kannangara C, Von Wettstein D, Hansson M (1999) Molecular basis for semidominance of missense mutations in the XANTHA-H (42-kDa) subunit of magnesium chelatase. Proc Natl Acad Sci USA 96:1744–1749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Homann PH, Schmid GH (1967) Photosynthetic reactions of chloroplasts with unusual structures. Plant Physiol 42:1619–1632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong J, Baek K, Kirst H, Melis A, Jin E (2017) Loss of CpSRP54 function leads to a truncated light-harvesting antenna size in Chlamydomonas reinhardtii. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1858(1):45–55

    Google Scholar 

  • Kirst H, Melis A (2014) The chloroplast Signal Recognition Particle pathway (CpSRP) as a tool to minimize chlorophyll antenna size and maximize photosynthetic productivity. Biotechnol Adv 32:66–72

    Article  CAS  PubMed  Google Scholar 

  • Kirst H, Garcia-Cerdan JG, Zurbriggen A, Melis A (2012a) Assembly of the light-harvesting chlorophyll antenna in the green alga Chlamydomonas reinhardtii requires expression of the TLA2-CpFTSY gene. Plant Physiol 158:930–945

    Article  CAS  PubMed  Google Scholar 

  • Kirst H, Garcia-Cerdan JG, Zurbriggen A, Ruehle T, Melis A (2012b) Truncated photosystem chlorophyll antenna size in the green microalga Chlamydomonas reinhardtii upon deletion of the TLA3-CpSRP43 gene. Plant Physiol 160(4):2251–2260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirst H, Formighieri C, Melis A (2014) Maximizing photosynthetic efficiency and culture productivity in cyanobacteria upon minimizing the phycobilisome light-harvesting antenna size. Biochim Biophys Acta Bioenerg 1837:1653–1664

    Article  CAS  Google Scholar 

  • Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354(6314):857–861

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Masuda T, Polle JEW, Melis A (2002) Biosynthesis and distribution of chlorophyll among the photosystems during recovery of the green alga Dunaliella salina from irradiance stress. Plant Physiol 128:603–614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melis A (1989) Spectroscopic methods in photosynthesis: photosystem stoichiometry and chlorophyll antenna size. Phil Trans R Soc Lond B 323:397–409

    Article  CAS  Google Scholar 

  • Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058:87–106

    Article  CAS  Google Scholar 

  • Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177:272–280

    Article  CAS  Google Scholar 

  • Melis A, Brown JS (1980) Stoichiometry of system I and system II reaction centers and of plastoquinone in different photosynthetic membranes. Proc Natl Acad Sci USA 77:4712–4716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melis A, Homann PH (1976) Heterogeneity of the photochemical centers in system II of chloroplasts. Photochem Photobiol 23:343–350

    Article  CAS  PubMed  Google Scholar 

  • Melis A, Thielen APGM (1980) The relative absorption cross-section of photosystem I and photosystem II in chloroplasts from three types of Nicotiana tabacum. Biochim Biophys Acta 589:275–286

    Article  CAS  PubMed  Google Scholar 

  • Melis A, Neidhardt J, Benemann JR (1999) Dunaliella salina (Chlorophyta) with small chlorophyll antenna sizes exhibit higher photosynthetic productivities and photon use efficiencies than normally pigmented cells. J Appl Phycol 10:515–525

    Article  Google Scholar 

  • Mitra M, Ng S, Melis A (2012) The TLA1 protein family members contain a variant of the plain MOV34/MPN domain. Am J Biochem Mol Biol 2(1):1–18

    Article  CAS  Google Scholar 

  • Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching: a response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed  PubMed Central  Google Scholar 

  • Mussgnug JH, Thomas-Hall S, Rupprecht J, Foo A, Klassen V, McDowall A, Schenk PM, Kruse O, Hankamer B (2007) Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion. Plant Biotechnol J 5:802–814

    Article  CAS  PubMed  Google Scholar 

  • Nakajima Y, Itayama T (2003) Analysis of photosynthetic productivity of microalgal mass cultures. J Appl Phycol 15:497–505

    Article  CAS  Google Scholar 

  • Nakajima Y, Ueda R (1997) Improvement of photosynthesis in dense microalgal suspension by reduction of light harvesting pigments. J Appl Phycol 9:503–510

    CAS  Google Scholar 

  • Nakajima Y, Ueda R (1999) Improvement of microalgal photosynthetic productivity by reducing the content of light harvesting pigments. J Appl Phycol 11:195–201

    Article  Google Scholar 

  • Nakajima Y, Tsuzuki M, Ueda R (2001) Improved productivity by reduction of the content of light-harvesting pigment in Chlamydomonas perigranulata. J Appl Phycol 13:95–101

    Article  CAS  Google Scholar 

  • Okabe K, Schmid GH, Straub J (1977) Genetic characterization and high efficiency photosynthesis of an aurea mutant of tobacco. Plant Physiol 60:150–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ort DR, Zhu XG, Melis A (2011) Optimizing antenna size to maximize photosynthetic efficiency. Plant Physiol 155:79–85

    Article  CAS  PubMed  Google Scholar 

  • Ort DR, Merchant SS, Alric J, Barkan A et al (2015) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Natl Acad Sci USA 112(28):8529–8536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polle JEW, Benemann JR, Tanaka A, Melis A (2000) Photosynthetic apparatus organization and function in wild type and a Chl b-less mutant of Chlamydomonas reinhardtii. Dependence on carbon source. Planta 211:335–344

    Article  CAS  PubMed  Google Scholar 

  • Polle JE, Kanakagiri SD, Melis A (2003) tla1, a DNA insertional transformant of the green alga Chlamydomonas reinhardtii with a truncated light-harvesting chlorophyll antenna size. Planta 217:49–59

    CAS  PubMed  Google Scholar 

  • Ruban AV (2016) Non-photochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protection against photodamage. Plant Physiol 170:1903–1916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shin WS, Lee BR, Chang YK, Kwon JH (2016) Truncated light-harvesting chlorophyll antenna size in Chlorella vulgaris improves biomass productivity. J Appl Phycol 28:3193–3202

    Article  CAS  Google Scholar 

  • Tetali SD, Mitra M, Melis A (2007) Development of the light-harvesting chlorophyll antenna in the green alga Chlamydomonas reinhardtii is regulated by the novel Tla1 gene. Planta 225:813–829

    Article  CAS  PubMed  Google Scholar 

  • Thielen APGM, van Gorkom HL (1981) Quantum efficiency and antenna size of photosystem II-alpha, II-beta and I in tobacco chloroplasts. Biochim Biophys Acta 635:111–120

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Hannah Clifton and Christina Wistrom for the greenhouse support they provided during the canopy-density experiments. Thanks are also due to Dr. Denise Schichnes for help with the microscopic leaf cross-section preparation and observations. The work was conducted as part of FOLIUM, a DOE ARPA-E PETRO project, Grant # AR0000204. K.K.N. is an investigator of the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (through Grant GBMF3070). PGL is supported by the U.S. Department of Agriculture Cooperative Extension Service through the University of California.

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Authors and Affiliations

  1. Department of Plant and Microbial Biology, University of California, 111 Koshland Hall, MC-3102, Berkeley, CA, 94720-3102, USA

    Henning Kirst, Stéphane T. Gabilly, Krishna K. Niyogi, Peggy G. Lemaux & Anastasios Melis

  2. Howard Hughes Medical Institute, University of California, Berkeley, CA, 94720-3102, USA

    Krishna K. Niyogi

  3. Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA

    Krishna K. Niyogi

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  1. Henning Kirst
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  2. Stéphane T. Gabilly
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  3. Krishna K. Niyogi
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  4. Peggy G. Lemaux
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  5. Anastasios Melis
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Correspondence to Anastasios Melis.

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Research did not involve Human and/or Animal Subjects. Experimental protocols in this work were approved by the UC Berkeley Committee on Laboratory and Environmental BioSafety (CLEB).

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Kirst, H., Gabilly, S.T., Niyogi, K.K. et al. Photosynthetic antenna engineering to improve crop yields. Planta 245, 1009–1020 (2017). https://doi.org/10.1007/s00425-017-2659-y

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