Planta

pp 1–16 | Cite as

Downregulation of the CpSRP43 gene expression confers a truncated light-harvesting antenna (TLA) and enhances biomass and leaf-to-stem ratio in Nicotiana tabacum canopies

  • Henning Kirst
  • Yanxin Shen
  • Evangelia Vamvaka
  • Nico Betterle
  • Dongmei Xu
  • Ujwala Warek
  • James A. Strickland
  • Anastasios Melis
Original Article
  • 71 Downloads

Abstract

Main conclusion

Downregulation in the expression of the signal recognition particle 43 (SRP43) gene in tobacco conferred a truncated photosynthetic light-harvesting antenna (TLA property), and resulted in plants with a greater leaf-to-stem ratio, improved photosynthetic productivity and canopy biomass accumulation under high-density cultivation conditions.

Evolution of sizable arrays of light-harvesting antennae in all photosynthetic systems confers a survival advantage for the organism in the wild, where sunlight is often the growth-limiting factor. In crop monocultures, however, this property is strongly counterproductive, when growth takes place under direct and excess sunlight. The large arrays of light-harvesting antennae in crop plants cause the surface of the canopies to over-absorb solar irradiance, far in excess of what is needed to saturate photosynthesis and forcing them to engage in wasteful dissipation of the excess energy. Evidence in this work showed that downregulation by RNA-interference approaches of the Nicotiana tabacum signal recognition particle 43 (SRP43), a nuclear gene encoding a chloroplast-localized component of the photosynthetic light-harvesting assembly pathway, caused a decrease in the light-harvesting antenna size of the photosystems, a corresponding increase in the photosynthetic productivity of chlorophyll in the leaves, and improved tobacco plant canopy biomass accumulation under high-density cultivation conditions. Importantly, the resulting TLA transgenic plants had a substantially greater leaf-to-stem biomass ratio, compared to those of the wild type, grown under identical agronomic conditions. The results are discussed in terms of the potential benefit that could accrue to agriculture upon application of the TLA-technology to crop plants, entailing higher density planting with plants having a greater biomass and leaf-to-stem ratio, translating into greater crop yields per plant with canopies in a novel agronomic configuration.

Keywords

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

Abbreviations

Car

Carotenoids

Chl

Chlorophyll

NPQ

Non-photochemical quenching

PS

Photosystem

TLA

Truncated light-harvesting antenna

TLA3-RNAi

Nicotiana tabacum TLA3-CpSRP43 gene downregulation of expression by RNA interference

Notes

Acknowledgements

We thank Hannah Clifton and Christina Wistrom for the greenhouse support they provided during the canopy density experiments. We also thank Dr. Peggy G. Lemaux for access to an ESL-1 cabinet and Dr. Krishna K. Niyogi for use of the LD2/3 electrode for oxygen evolution measurements.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human participants and/or animals

Research did not involve human and/or animal subjects. Experimental protocols in this work were approved by the UC Berkeley Committee for Laboratory and Environmental BioSafety (CLEB).

Informed consent

All authors have read and approved submission of this work.

Supplementary material

425_2018_2889_MOESM1_ESM.pdf (10.5 mb)
Supplementary material 1 (PDF 10729 kb)

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. 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
  3. Bonente G, Formighieri C, Mantelli M, Catalanotti C, Giuliano G, Morosinotto T, Bassi R (2011) Mutagenesis and phenotypic selection as a strategy toward domestication of Chlamydomonas reinhardtii strains for improved performance in photobioreactors. Photosynth Res 108(2–3):107–120CrossRefPubMedGoogle Scholar
  4. 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
  5. Dall’Osto L, Cazzaniga S, Bressan M, Paleček D, Židek K, Niyogi KK, Fleming GR, Zigmantas D, Bassi R (2017) Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes. Nat Plants 3:17033CrossRefPubMedGoogle Scholar
  6. Droppa M, Ghirardi ML, Horvath G, Melis A (1988) Chlorophyll b-deficiency in soybean mutants. II. Thylakoid membrane development and differentiation. Biochim Biophys Acta 932:138–145CrossRefGoogle Scholar
  7. 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
  8. 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
  9. 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
  10. Glazer AN, Melis A (1987) Photochemical reaction centers: structure, organization, and function. Annu Rev Plant Physiol 38:11–45CrossRefGoogle Scholar
  11. Glick RE, Melis A (1988) Minimum photosynthetic unit size in system I and system II of barley chloroplasts. Biochim Biophys Acta 934:151–155CrossRefGoogle 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. Hiyama T, Ke B (1972) Difference spectra and extinction coefficients of P 700. Biochim Biophys Acta (BBA) Bioenerg 267:160–171CrossRefGoogle Scholar
  15. Homann PH, Schmid GH (1967) Photosynthetic reactions of chloroplasts with unusual structures. Plant Physiol 42:1619–1632CrossRefPubMedPubMedCentralGoogle Scholar
  16. Jansson S (1994) The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta 1184(1):1–19CrossRefPubMedGoogle Scholar
  17. Jansson S, Pichersky E, Bassi R, Green BR, Ikeuchi M, Melis A, Simpson DJ, Spangfort M, Staehelin LA, Thornber JP (1992) A nomenclature for the genes encoding the chlorophyll ab-binding proteins of higher plants. Plant Mol Biol Rep 10:242–253CrossRefGoogle Scholar
  18. 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. Biochim Biophys Acta 1858:45–55CrossRefPubMedGoogle Scholar
  19. Jeong J, Baek K, Jihyeon YuJ, Kirst H, Betterle N, Shin W, Bae S, Melis A, Jin ES (2018) Deletion of the chloroplast LTD protein impedes LHCI import and PSI-LHCI assembly in Chlamydomonas reinhardtii. J Exp Bot 69:1147–1158CrossRefGoogle Scholar
  20. Kirst H, Melis A (2014) The chloroplast Signal Recognition Particle pathway (CpSRP) as a tool to minimize chlorophyll antenna size and maximize photosynthetic productivity. Biotech Adv 32:66–72CrossRefGoogle Scholar
  21. Kirst H, Melis A (2018) Improving photosynthetic solar energy conversion efficiency: the truncated light-harvesting antenna (TLA) concept. In: Seibert M, Torzillo G (eds) Microalgal hydrogen production: achievements and perspectives, chap 14. European Society for Photobiology 2018. Royal Society of Chemistry, London, pp 335–353Google Scholar
  22. 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
  23. 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
  24. 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
  25. Kirst H, Gabilly ST, Niyogi KK, Lemaux PG, Melis A (2017) Photosynthetic antenna engineering to improve crop yields. Planta 245:1009–1020CrossRefPubMedGoogle Scholar
  26. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMedGoogle Scholar
  27. Lea-Smith DJ, Bombelli P, Dennis JS, Scott SA, Smith AG, Howe CJ (2014) Phycobilisome deficient strains of Synechocystis sp PCC6803 have reduced size and require carbon limiting conditions to exhibit enhanced productivity. Plant Physiol 165:705–714CrossRefPubMedPubMedCentralGoogle Scholar
  28. Liberton M, Collins AM, Page LE, O’Dell WO, O’Neill H, Urban WS, Timlin JA, Pakrasi HB (2013) Probing the consequences of antenna modification in cyanobacteria. Photosynth Res 118:17–24CrossRefPubMedGoogle Scholar
  29. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382CrossRefGoogle Scholar
  30. 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
  31. Melis A (1989) Spectroscopic methods in photosynthesis: photosystem stoichiometry and chlorophyll antenna size. Philos Trans R Soc Lond B 323:397–409CrossRefGoogle Scholar
  32. Melis A (1990) Regulation of photosystem stoichiometry in oxygenic photosynthesis. In: Kanai R, Katoh S, Miyachi S (eds) Regulation of photosynthetic processes. Botanical magazine Tokyo, special issue vol 2. University of Tokyo Press, Tokyo, pp 9–28Google Scholar
  33. Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058:87–106CrossRefGoogle Scholar
  34. Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177:272–280CrossRefGoogle Scholar
  35. 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
  36. 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
  37. 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
  38. 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
  39. Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching: a response to excess light energy. Plant Physiol 125:1558–1566CrossRefPubMedPubMedCentralGoogle Scholar
  40. Mussgnug JH, Wobbe L, Elles I, Claus C, Hamilton M, Fink A, Kahmann U, Kapazoglou A, Mullineaux CW, Hippler M, Nickelsen J, Nixon PJ, Kruse O (2005) NAB1 is an RNA binding protein involved in the light-regulated differential expression of the light-harvesting antenna of Chlamydomonas reinhardtii. Plant Cell 17:3409–3421CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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 Biotech J 5:802–814CrossRefGoogle Scholar
  42. Nakajima Y, Itayama T (2003) Analysis of photosynthetic productivity of microalgal mass cultures. J Appl Phycol 15:450–497CrossRefGoogle Scholar
  43. 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
  44. 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
  45. Nakajima Y, Ueda R (2000) The effect of reducing light-harvesting pigment on marine microalgal productivity. J Appl Phycol 12(3–5):285–290CrossRefGoogle Scholar
  46. 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
  47. 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
  48. Ort DR, Zhu XG, Melis A (2011) Optimizing antenna size to maximize photosynthetic efficiency. Plant Physiol 155:79–85CrossRefPubMedGoogle Scholar
  49. Page LE, Liberton M, Pakrasi H (2012) Reduction of photoautotrophic productivity in the cyanobacterium Synechocystis sp strain PCC 6803 by phycobilisome antenna truncation. Appl Environ Microbiol 78:6349–6351CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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
  51. 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
  52. Ruban AV (2016) Non-photochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protection against photodamage. Plant Physiol 170:1903–1916CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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
  54. Slattery RA, VanLoocke A, Bernacchi CJ, Zhu XG, Ort DR (2017) Photosynthesis, light use efficiency, and yield of reduced-chlorophyll soybean mutants in field conditions. Front Plant Sci 8:549CrossRefPubMedPubMedCentralGoogle Scholar
  55. Song Q, Wang Y, Qu M, Ort DR, Zhu XG (2017) The impact of modifying photosystem antenna size on canopy photosynthetic efficiency-development of a new canopy photosynthesis model scaling from metabolism to canopy level processes. Plant Cell Environ 40:2946–2957CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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
  57. 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
  58. Van Gorkom HJ (1974) Identification of the reduced primary electron acceptor of photosystem II as a bound semiquinone anion. Biochim Biophys Acta 347:439–442CrossRefPubMedGoogle Scholar
  59. Walker BJ, Drewry DT, Slattery RA, VanLoocke A, Cho YB, Ort DR (2017) Chlorophyll can be reduced in crop canopies with little penalty to photosynthesis. Plant Physiol.  https://doi.org/10.1104/pp.17.01401 Google Scholar
  60. Wobbe L, Bassi R, Kruse O (2016) Multi-level light capture control in plants and green algae. Trends Plant Sci 21(1):55–68CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Plant and Microbial BiologyUniversity of CaliforniaBerkeleyUSA
  2. 2.Biotechnology DivisionAltria Client ServicesRichmondUSA

Personalised recommendations