Planta

, Volume 245, Issue 5, pp 1009–1020 | Cite as

Photosynthetic antenna engineering to improve crop yields

  • Henning Kirst
  • Stéphane T. Gabilly
  • Krishna K. Niyogi
  • Peggy G. Lemaux
  • Anastasios Melis
Original Article

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.

Keywords

Chlorophyll-deficient mutant Canopy density Light-harvesting antenna size Nicotiana tabacum Productivity TLA technology 

Abbreviations

Car

Carotenoids

PS

Photosystem

TLA

Truncated light-harvesting antenna

References

  1. Abadia J, Glick RE, Taylor SE, Terry N, Melis A (1985) Photochemical apparatus organization in the chloroplasts of two Beta vulgaris genotypes. Plant Physiol 79:872–878CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alexandratos N, Bruinsma J (2012) World Agriculture: Towards 2030/2050. The 2012 revision. ESA Working Paper No. 12-03, Food Agric Org, RomeGoogle Scholar
  3. Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annu Rev Plant Physiol 37:93–136CrossRefGoogle Scholar
  4. 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 8:277–287CrossRefPubMedGoogle Scholar
  5. Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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):157CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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 27:1063–1077CrossRefGoogle Scholar
  8. 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 153:1919–1928PubMedPubMedCentralGoogle Scholar
  9. Ghirardi ML, Melis A (1988) Chlorophyll b-deficiency in soybean mutants. I. Effects on photosystem stoichiometry and chlorophyll antenna size. Biochim Biophys Acta 932:130–137CrossRefGoogle Scholar
  10. 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 851:331–339CrossRefGoogle Scholar
  11. 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 327:812–818CrossRefPubMedGoogle Scholar
  12. Greene BA, Staehelin LA, Melis A (1988) Compensatory alterations in the photochemical apparatus of a photoregulatory, chlorophyll b-deficient mutant of maize. Plant Physiol 87:365–370CrossRefPubMedPubMedCentralGoogle Scholar
  13. 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 96:1744–1749CrossRefPubMedPubMedCentralGoogle Scholar
  14. Homann PH, Schmid GH (1967) Photosynthetic reactions of chloroplasts with unusual structures. Plant Physiol 42:1619–1632CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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):45–55Google Scholar
  16. 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 32:66–72CrossRefPubMedGoogle Scholar
  17. 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 158:930–945CrossRefPubMedGoogle Scholar
  18. 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):2251–2260CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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 1837:1653–1664CrossRefGoogle Scholar
  20. 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):857–861CrossRefPubMedGoogle Scholar
  21. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382CrossRefGoogle Scholar
  22. 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 128:603–614CrossRefPubMedPubMedCentralGoogle Scholar
  23. Melis A (1989) Spectroscopic methods in photosynthesis: photosystem stoichiometry and chlorophyll antenna size. Phil Trans R Soc Lond B 323:397–409CrossRefGoogle Scholar
  24. Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058:87–106CrossRefGoogle Scholar
  25. Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177:272–280CrossRefGoogle Scholar
  26. 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 77:4712–4716CrossRefPubMedPubMedCentralGoogle Scholar
  27. Melis A, Homann PH (1976) Heterogeneity of the photochemical centers in system II of chloroplasts. Photochem Photobiol 23:343–350CrossRefPubMedGoogle Scholar
  28. 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 589:275–286CrossRefPubMedGoogle Scholar
  29. 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 10:515–525CrossRefGoogle Scholar
  30. 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):1–18CrossRefGoogle Scholar
  31. Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching: a response to excess light energy. Plant Physiol 125:1558–1566CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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 5:802–814CrossRefPubMedGoogle Scholar
  33. Nakajima Y, Itayama T (2003) Analysis of photosynthetic productivity of microalgal mass cultures. J Appl Phycol 15:497–505CrossRefGoogle Scholar
  34. Nakajima Y, Ueda R (1997) Improvement of photosynthesis in dense microalgal suspension by reduction of light harvesting pigments. J Appl Phycol 9:503–510Google Scholar
  35. Nakajima Y, Ueda R (1999) Improvement of microalgal photosynthetic productivity by reducing the content of light harvesting pigments. J Appl Phycol 11:195–201CrossRefGoogle Scholar
  36. Nakajima Y, Tsuzuki M, Ueda R (2001) Improved productivity by reduction of the content of light-harvesting pigment in Chlamydomonas perigranulata. J Appl Phycol 13:95–101CrossRefGoogle Scholar
  37. Okabe K, Schmid GH, Straub J (1977) Genetic characterization and high efficiency photosynthesis of an aurea mutant of tobacco. Plant Physiol 60:150–156CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ort DR, Zhu XG, Melis A (2011) Optimizing antenna size to maximize photosynthetic efficiency. Plant Physiol 155:79–85CrossRefPubMedGoogle Scholar
  39. 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):8529–8536CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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 211:335–344CrossRefPubMedGoogle Scholar
  41. 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 217:49–59PubMedGoogle Scholar
  42. Ruban AV (2016) Non-photochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protection against photodamage. Plant Physiol 170:1903–1916CrossRefPubMedPubMedCentralGoogle Scholar
  43. Shin WS, Lee BR, Chang YK, Kwon JH (2016) Truncated light-harvesting chlorophyll antenna size in Chlorella vulgaris improves biomass productivity. J Appl Phycol 28:3193–3202CrossRefGoogle Scholar
  44. 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 225:813–829CrossRefPubMedGoogle Scholar
  45. 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 635:111–120CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Henning Kirst
    • 1
  • Stéphane T. Gabilly
    • 1
  • Krishna K. Niyogi
    • 1
    • 2
    • 3
  • Peggy G. Lemaux
    • 1
  • Anastasios Melis
    • 1
  1. 1.Department of Plant and Microbial BiologyUniversity of CaliforniaBerkeleyUSA
  2. 2.Howard Hughes Medical InstituteUniversity of CaliforniaBerkeleyUSA
  3. 3.Molecular Biophysics and Integrated Bioimaging DivisionLawrence Berkeley National LaboratoryBerkeleyUSA

Personalised recommendations