Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2017, Vol. 52, № 5, p. 843-855
(how to cite this article).

doi: 10.15389/agrobiology.2017.5.843eng

UDC 631.522/.524:581.132.1:57.05

Acknowlegdgements:
Supported by Russian Science Foundation (grant № 14-16-00120)

 

CHLOROPHYLL B AS A SOURCE OF SIGNALS STEERING PLANT
DEVELOPMENT (review)

E.V. Tyutereva, V.A. Dmitrieva, O.V. Voitsekhovskaja

Laboratory of Molecular and Ecological Physiology, V.L. Komarov Botanical Institute RAS, Federal Agency of Scientific Organizations, 2, ul. Professora Popova, St. Petersburg, 197376 Russia, e-mail ETutereva@binran.ru, VDmitrieva@binran.ru, ovoitse@binran.ru (corresponding author);

ORCID:
Tyutereva E.V. orcid.org/0000-0002-6727-6656
Dmitrieva V.A. orcid.org/0000-0002-7293-0229
Voitsekhovskaja O.V. orcid.org/0000-0003-0966-1270

Received December 12, 2016

Crop yield strongly depends on time of the onset of flowering as well as of the initiation of senescence. These processes are under tight control of multiple gene complexes. Suboptimal environmental conditions, as well as mutations, may cause changes in the expression levels of these genes, which, in turn, can result in a delay of flowering and/or early senescence, and, ultimately, in a decrease of yield. Recently, crucial role in the regulation of plant development via retrograde signaling pathways has been revealed for chlorophyll b. Chlorophyll b is an obligate component of the photosynthetic apparatus of land plants, and the main regulator of the biosynthesis and degradation of photosynthetic antennae. It is becoming clear that the size and stability of photosynthetic antennae is not only important for photosynthesis but also represents a source of signaling beyond chloroplasts. The absence of chlorophyll bin mutants of Arabidopsis thaliana (ch1) and Hordeum vulgare (chlorina f2 3613) leads to a decrease in the growth rate, leaf size and biomass production. In addition, and independently of the downregulation of photosynthesis, the lack of chlorophyll b results in the delay of flowering and early onset of ontogenetic as well as induced senescence. This review addresses the role of chlorophyll b in energy balance, and discusses new data on the role of chlorophyll b in regulation of ontogenesis not related to photosynthesis. Mutants of economically important crops impaired in chlorophyll b biosynthesis represent promising models for physiological, biochemical and molecular studies of regulation of flowering and senescence, as the results can be directly applied to agricultural practice. Also, we review the novel data on the potential importance of plants with truncated photosynthetic antenna for increase in vegetative and grain biomass production. A decrease in chlorophyll b contents and the following down-regulation of antenna proteins were shown to influence the rate of electron transport within the photosystem II, as well as the rate of CO2 assimilation relative to chlorophyll unit. Strikingly, these parameters in chlorina mutants are higher than in wild type plants by 15-20 %. Using plants with this type of photosynthetic apparatus can potentially bring about a considerable increase in yield. This suggestion has been recently supported by data on transgenic tobacco plants with truncated photosynthetic antenna (H. Kirst et al. 2017). At the same time, the consequences of the decrease in chlorophyll b levels for ontogenetic regulation and photoprotection typically negate the potential benefit of the acceleration of the limiting factor of photosynthesis, the photosystem II. This review discuss the possible ways to search for optimization of plant functions regulated by chlorophyll b, to provide new mechanisms of the increase in photosynthesis and crop production in agriculture.

Keywords: yield, chlorophyll b, flowering, ontogenesis, senescence, photosynthetic antenna.

 

Full article (Rus)

Full text (Eng)

 

REFERENCES

  1. Simpson G.G., Dean C. Arabidopsis, the rosetta stone of flowering time? Science, 2002, 296: 285-289 CrossRef
  2. Mathieu J., Warthmann N., Kuttner F., Schmid M. Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr. Biol., 2007, 17: 1055-1060 CrossRef
  3. Peng F.Y., Hu Z., Yang R.C. Genome-wide comparative analysis of flowering-related genes in Arabidopsis, wheat and barley. Int. J. Plant Genomics, 2015, 2015: 874361 CrossRef
  4. Koornneef M., Alonso-Blanco C., Peeters A.J.M., Soppev W. Genetic control of flowering time in Arabidopsis. Physiol. Plant. Mol. Biol., 1998, 49: 345-370 CrossRef
  5. Schulze W., Schulze E.-D., Stadler J., Heilmeier H., Stitt M., Mooney H.A. Growth and reproduction of Arabidopsis thaliana in relation to storage of starch and nitrate in the wild-type and in starch-deficient and nitrate-uptake-deficient mutants. Plant, Cell & Environment, 1994, 17(7): 795-809 CrossRef
  6. Kojima S., Takahashi Y., Kobayashi Y., Monna L., Sasaki T., Araki T., Yano M. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol., 2002, 43(10): 1096-1105 CrossRef
  7. Putterill J., Robson F., Lee K., Simon R., Coupland G. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell, 1995, 80: 847-857 CrossRef
  8. Jaeger K.E., Wigge P.A. FT protein acts as a long-range signal in Arabidopsis. Current Biology, 2007, 17: 1050-1054 CrossRef
  9. Kardailsky I., Shukla V.K., Ahn J.H., Dagenais N., Christensen S.K., Nguyen J.T., Chory J., Harrison M.J., Detlef W. Activation tagging of the floral inducer FT. Science, 1999, 286: 1962-1865 CrossRef
  10. Becker A., Ehlers K. Arabidopsis flower development—of protein complexes, targets, and transport. Protoplasma, 2015, 253: 219-230 CrossRef
  11. Vaddepalli P., Scholz S., Schneitz K. Pattern formation during early floral development. Curr. Opin. Genet. Dev., 2015, 32: 16-23 CrossRef
  12. Pineiro M., Coupland G. The control of flowering time and floral identity in Arabidopsis. Plant Physiol., 1998, 117: 1-8 CrossRef
  13. Corbesier L., Vincent C., Jang S., Fornara F., Fan Q., Searle I., Giakountis A., Farrona S., Gissot L., Turnbull C., Coupland G. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science, 2007, 316: 1030-1033 CrossRef
  14. Gregersen P.L., Culetic A., Boschian L., Krupinska K. Plant senescence and crop productivity. Plant Mol. Biol., 2013, 82: 603-622 CrossRef
  15. Nam H.G. The molecular genetic analysis of leaf senescence. Current Opinion in Biotechnology, 1997, 8(2): 200-207 CrossRef
  16. Buchanan-Wollaston V., Earl S., Harrison E., Mathas E., Navabpour S., Page T., Pink D. The molecular analysis of leaf senescence — a genomics approach. Plant Biotechnology Journal, 2003, 1(1): 3-22 CrossRef
  17. Lim P.O., Kim Y., Breeze E., Koo J.C., Woo H.R., Ryu J.S., Park D.H., Beynon J., Tabrett A., Buchanan-Wollaston V., Nam H.G. Overexpression of a chromatin architecture-controlling AT-hook protein extends leaf longevity and increases the post-harvest storage life of plants. The Plant Journal, 2007, 52(6): 1140-1153 CrossRef
  18. Hopkins M., Taylor C., Liu Z., Ma F., McNamara L., Wang T., Thompson J.E. Regulation and execution of molecular disassembly and catabolism during senescence. New Phytologist, 2007, 175(2): 201-214 CrossRef
  19. Jansson S., Thomas H. Senescence: developmental program or timetable? New Phytologist, 2008, 179(3): 575-579 CrossRef
  20. Buchanan-Wollaston V., Ainsworth C. The molecular biology of leaf senescence. J. Exp. Bot., 1997, 48(307): 181-199 CrossRef
  21. Hollmann J., Gregersen P.L., Krupinska K. Identification of predominant genes involved in regulation and execution of senescence-associated nitrogen remobilization in flag leaves of field grown barley. J. Exp. Bot., 2014, 65(14): 3963-3973 CrossRef
  22. Noodén L.D., Penney J.P. Correlative controls of senescence and plant death in Arabidopsis thaliana (Brassicaceae). J. Exp. Bot., 2001, 52(364): 2151-2159 CrossRef
  23. Zapata J.M., Guéra A., Esteban-Carrasco A., Martín M., Sabater B. Chloroplasts regulate leaf senescence: delayed senescence in transgenic ndhF-defective tobacco. Cell Death and Differentiation, 2005, 12: 1277-1284 CrossRef
  24. Parrott D.L., Martin J.M., Fischer A.M. Analysis of barley (Hordeum vulgare) leaf senescence and protease gene expression: a family C1A cysteine protease is specifically induced under conditions characterized by high carbohydrate, but low to moderate nitrogen levels. New Phytologist, 2010, 187(2): 313-331 CrossRef
  25. Buchanan-Wollaston V. The molecular biology of leaf senescence. J. Exp. Bot., 1997, 48(307): 181-199 CrossRef
  26. Jukanti A.K., Heidlebaugh N.M., Parrott D.L., Fischer I.A., McInnerney K., Fischer A.M. Comparative transcriptome profiling of near-isogenic barley (Hordeum vulgare) lines differing in the allelic state of a major grain protein content locus identifies genes with possible roles in leaf senescence and nitrogen reallocation. New Phytologist, 2008, 177(2): 333-349 CrossRef
  27. Buchanan-Wollaston V., Page T., Harrison E., Breeze E., Lim P.O., Nam H.G., Ji-Feng L., Shu-Hsing W., Jodi S., Kimitsune I., Christopher J. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. The Plant Journal, 2005, 42: 567-585 CrossRef
  28. Gepstein S., Sabehi G., Carp M.J., Hajouj T., Falah M., Nesher O., Yariv I., Dor C., Bassani M. Large-scale identification of leaf senescence-associated genes. The Plant Journal, 2003, 36(5): 629-642 CrossRef
  29. Grbic V., Bleecker A.B. Ethylene regulates the timing of leaf senescence in Arabidopsis. The Plant Journal, 1995, 8(4): 595-602 CrossRef
  30. Guo Y., Gan S. Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments. Plant Cell Environ., 2012, 35: 644-655 CrossRef
  31. Noh Y., Amasino R.M. Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol. Biol., 1999, 41: 181-194 CrossRef
  32. He Y., Gan S. A gene encoding an acyl hydrolase is involved in leaf senescence in Arabidopsis. The Plant Cell, 2002, 14: 805-815 CrossRef
  33. Xiao W.S., Gao W., Chen Q.-F., Chan S.-W., Zheng S.-X., Ma J., Wang M., Welti R., Chye M.-L. Overexpression of Arabidopsis acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence. The Plant Cell, 2010, 22: 1463-1482 CrossRef
  34. Hirashima M., Satoh S., Tanaka R., Tanaka A. Pigment shuffling in antenna systems achieved by expressing prokaryotic chlorophyllide a oxygenase in Arabidopsis. J. Biol. Chem., 2006, 281: 15385-15393 CrossRef
  35. Sakuraba Y., Balazadeh S., Tanaka R., Mueller-Roeber B., Tanaka A. Overproduction of chl b retards senescence through transcriptional reprogramming in Arabidopsis. Plant Cell Physiol., 2012, 53: 505-517 CrossRef
  36. Tyutereva E.V., Ivanova A.N., Voitsekhovskaya O.V. Uspekhi sovremennoi biologii, 2014, 134: 249-256 (in Russ.).
  37. Tomitani A., Okada K., Miyashita H., Matthijs H.C.P., Ohno T., Tanaka A. Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts. Nature, 1999, 400: 159-162 CrossRef
  38. Sakuraba Y., Yokono M., Akimoto S., Tanaka R., Tanaka A. Deregulated chlorophyll b synthesis reduces the energy transfer rate between photosynthetic pigments and induces photodamage in Arabidopsis thaliana. Plant Cell Physiol., 2010, 51: 1055-1065 CrossRef
  39. Espineda C.E., Alicia S.L., Domenica D., Brusslan J.A. The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b. PNAS USA, 1999, 96: 10507-10511 CrossRef
  40. Beale S.I. Enzymes of chlorophyll biosynthesis. Photosynthesis Research, 1999, 60: 43-73 CrossRef
  41. Nakagawara E., Sakuraba Y., Yamasato A., Tanaka R., Tanaka A. Clp protease controls chlorophyll b synthesis by regulating the level of chlorophyllide a oxygenase. Plant J., 2007, 49: 800-809 CrossRef
  42. Yamasato A., Nagata N., Tanaka R., Tanaka A. The N-terminal domain of chlorophyllide a oxygenase confers protein instability in response to chlorophyll b accumulation in Arabidopsis. The Plant Cell, 2005, 17: 1585-1597 CrossRef
  43. Bailey S., Walters R.G., Jansson S., Horton P. Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta, 2001, 213: 794-801 CrossRef
  44. Voitsekhovskaja O.V., Tyutereva E.V. Chlorophyll b in angiosperms: functions in photosynthesis, signaling and ontogenetic regulation. J. Plant Physiol., 2015, 189: 51-64 CrossRef
  45. Tanaka R., Tanaka A. Chlorophyll cycle regulates the construction and destruction of the light-harvesting complexes. BBA, 2011, 1807: 968-976 CrossRef
  46. Croce R., Muller M.G., Bassi R., Holzwarth A.R. Carotenoid-to-chlorophyll energy transfer in recombinant major light-harvesting complex (LHCII) of higher plants. I. Femtosecond transient absorption measurements. Biophys. J., 2001, 80: 901-915 CrossRef
  47. Walla P.J., Yom J., Krueger B.P., Fleming G.R. Two-photon excitation spectrum of light-harvesting complex II and fluorescence upconversion after one- and twophoton excitation of the carotenoids. J. Phys. Chem. B, 2000, 104: 4799-4806 CrossRef
  48. Novoderezhkin V.I., Palacios M.A., van Amerongen H., van Grondelle R. Excitation dynamics in the LHCII complex of higher plants: modeling based on the 2.72 Angstrom crystal structure. J. Phys. Chem. B, 2005, 109: 10493-10504 CrossRef
  49. Schlau-Cohen G.S., Calhoun T.R., Ginsberg N.S., Read E.L., Ballottari M., Bassi R., van Grondelle R., Fleming G.R. Pathways of energy flow in LHCII from two dimensional electronic spectroscopy. J. Phys. Chem. B, 2009, 113: 15352-15363 CrossRef
  50. Formaggio E., Cinque G., Bassi R. Functional architecture of the major light-harvesting complex from higher plants. J. Mol. Biol., 2001, 314: 1157-1166 CrossRef
  51. Croce R., Zucchelli G., Garlaschi F.M., Jennings R.C. A thermal broadening study of the antenna chlorophylls in PSI-200, LHCI, and PSI core. Biochemistry, 1998, 37: 17355-17360 CrossRef
  52. Rivadossi A., Zucchelli G., Garlaschi F.M., Jennings R.C. The importance of PSI chlorophyll red forms in light-harvesting by leaves. Photosynth. Res., 1999, 60: 209-215.
  53. Avenson T.J., Ahn T.K., Zigmantas D., Niyogi K.K., Li Z., Ballottari M., Bassi R., Fleming G.R. Zeaxanthin radical formation in minor light-harvesting complexes of higher plant antenna. J. Biol. Chem., 2008, 283: 3550-3558 CrossRef
  54. Ballottari M., Mozzo M., Girardon J., Hienerwadel R., Bassi R. Chlorophyll triplet quenching and photoprotection in the higher plant monomeric antenna protein Lhcb5. J. Phys. Chem. B, 2013, 117(38): 11337-11348 CrossRef
  55. Dall'osto L., Cazzaniga S., Havaux M., Bassi R. Enhanced photoprotection by protein-bound vs free xanthophyll pools: a comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants. Molecular Plant, 2010, 3: 576-593 CrossRef
  56. Ramel F., Ksas B., Akkari E., Mialoundama A.S., Monnet F., Krieger-Liszkay A., Ravanat J.-L., Mueller M.J., Bouvier F., Havaux M. Light-induced acclimation of the Arabidopsis chlorina1 mutant to singlet oxygen. The Plant Cell, 2013, 25: 1445-1462 CrossRef
  57. Tyutereva E.V., Evkaikina A.I., Ivanova A.N., Voitsekhovskaja O.V. The absence of chlorophyll b affects lateral mobility of photosynthetic complexes and lipids in grana membranes of Arabidopsis and barley chlorina mutants. Photosynthesis Research, 2017, 113: 357-370 CrossRef
  58. Tanaka A., Ito H., Tanaka R., Tanaka N.K., Yoshida K., Okada K. Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. PNAS, 1998, 95(21): 12719-12723 CrossRef
  59. Hoober J.K., Eggink L.L., Chen M. Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts. Photosynthesis Research, 2007, 94: 387-400 CrossRef
  60. Klimmek F., Sjodin A., Noutsos C., Leister D., Jansson S. Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants. Plant Physiol., 2006, 140: 793-804 CrossRef
  61. Mishra S.R., Eu Y., Nath K., Tovu A., Zulfugarov I.S., Lee C.-H. Mutants of chlorophyllide oxygenase. In: Photosynthesis: overviews on recent progress & future perspective. S. Itoh, P. Mohanty, K.N. Guruprasad (eds.). IK International Publishing House, 2012: 130-145.
  62. Humbeck K., Quast S., Krupinska K. Functional and molecular changes in the photosynthetic apparatus during senescence of flag leaves from field-grown barley plants. Plant, Cell and Environment, 1996, 19: 337-344 CrossRef
  63. Hortensteiner S., Feller U. Nitrogen metabolism and remobilization during senescence. J. Exp. Bot., 2002, 53; 370: 927-937 CrossRef
  64. Hortensteiner S., Vicentini F., Matile P. Chlorophyll breakdown in senescent cotyledons of rape, Brassica napus L.: enzymatic cleavage of phaeophorbide a in vitro. New Phytologist, 1995, 129: 237-246 CrossRef
  65. Kusaba M., Ito H., Morita R., Iida S., Sato Y., Fujimoto M. Rice NON-YELLOW COLORING1 is involved in light-harvesting complex 2 and grana degradation during leaf senescence. Plant Cell, 2007, 19: 1362-1375 CrossRef
  66. Jia T, Ito H, Hu X, Tanaka A. Accumulation of the NON-YELLOW COLORING 1 protein of the chlorophyll cycle requires chlorophyll b in Arabidopsis thaliana. Plant J., 2015, 81: 586-596 CrossRef
  67. Kim E.H., Li X.P., Razeghifard R., Anderson J.M., Niyogi K.K., Pogson B.J., Chow W.S. The multiple roles of light-harvesting chlorophyll a/b-protein complexes define structure and optimize function of Arabidopsis chloroplasts: a study using two chlorophyll b-less mutants. BBA, 2009, 1787: 973-984 CrossRef
  68. Bianchi S., Dall’osto L., Tognon G., Morosinotto T., Bassi R. Minor antenna proteins CP24 and CP26 affect the interactions between photosystem II subunits and the electron transport rate in grana membranes of Arabidopsis. Plant Cell, 2008, 20: 1012-1028 CrossRef
  69. Goral T.K., Johnson M.P., Duffy C.D.P., Brain A.P.R, Ruban A.V., Mullineaux C.W. Light-harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis. Plant J., 2012, 69: 289-301 CrossRef
  70. Miller K.R., Miller G.J., McIntyre K.R. The light-harvesting chlorophyll-protein complex of photosystem II. Its location in the photosynthetic membrane. J. Cell Biol., 1976, 71: 624-638 CrossRef
  71. Kirchhoff H. Diffusion of molecules and macromolecules in thylakoid membranes. BBA, 2014, 1837: 495-502 CrossRef
  72. Pesaresi P., Schneider A., Kleine T., Leister D. Interorganellar communication. Curr. Opin. Plant Biol., 2007, 10(6): 600-606 CrossRef
  73. Baier M., Dietz K.-J. Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology. J. Exp. Bot., 2005, 56(416): 1449-1462 CrossRef
  74. Jung H.-S., Chory J. Signaling between chloroplasts and the nucleus: can a systems biology approach bring clarity to a complex and highly regulated pathway? Plant Physiol., 2010, 152: 453-459 CrossRef
  75. Kleine T., Voigt C., Leister D. Plastid signalling to the nucleus: messengers still lost in the mists? Trends Genet., 2009, 25: 185-192 CrossRef
  76. Kobayashi Y., Kanesaki Y., Tanaka A., Kuroiwa H., Kuroiwa T., Tanaka R. Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells. PNAS USA, 2009, 106: 803-807 CrossRef
  77. Horie Y., Ito H., Kusaba M., Tanaka R., Tanaka A. Participation of chlorophyll b reductase in the initial step of the degradation of light-harvesting chlorophyll a/b-protein complexes in Arabidopsis. J. Biol. Chem., 2009, 284: 17449-17456 CrossRef
  78. Sakuraba Y., Kim Y.S., Yoo S.C., Hörtensteiner S., Paek N.C. 7-Hydroxymethyl chlorophyll a reductase functions in metabolic channeling of chlorophyll breakdown intermediates during leaf senescence. Biochem. Bioph. Res. Co., 2013, 430: 32-37 CrossRef
  79. Reumann S., Voitsekhovskaja O., Lillo C. From signal transduction to autophagy of plant cell organelles: lessons from yeast and mammals and plant-specific features. Protoplasma, 2010, 247: 233-256 CrossRef
  80. Sakuraba Y., Lee S.-H., Kim Y.S., Park O.K., Hörtensteiner S., Paek N.C. Delayed degradation of chlorophylls and photosyhthetic proteins in Arabidopsis autophagy mutants during stress-induced leaf yellowing. J. Exp. Bot., 2014, 65: 3915-3925 CrossRef
  81. Dmitrieva V.A. Rol' stabilizatsii pigment-belkovykh kompleksov fotosinteticheskogo apparata v regulyatsii tsveteniya Hordeum vulgare i Arabidopsis thaliana (vypusknaya kvalifikatsionnaya rabota) [The role of stability of photosynthetic pigment-protein complexes in regulation of flowering in Hordeum vulgare and Arabidopsis thaliana].St. Petersburg, 2016 (in Russ.).
  82. Kromdijk J., Glowacka K., Leonelli L., Gabilly S.T., Iwai M., Niyogi K.K., Long S. Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science, 2016, 354: 857-861 CrossRef
  83. Kirst H., Gabilly S.T., Niyogi K.K., Lemaux P.G., Melis A. Photosynthetic antenna engineering to improve crop yields. Planta, 2017, 245: 1009-1020 CrossRef
  84. Brestic M., Zivcak M., Kunderlikova K., Sytar O., Shao H., Kalaji H.M., Allakhverdiev S.I. Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. Planta, 2015, 125: 151-166 CrossRef
  85. Brestic M., Zivcak M., Kunderlikova K., Allakhverdiev S.I. High temperature specifically affects the photoprotective responses of chlorophyll b-deficient wheat mutant lines. Planta, 2016, 130: 251-366 CrossRef
  86. Slattery R., VanLoocke A., Bernacchi K.J., Zhu X.-G., Ort D.R. Photosynthesis, light use efficiency and yield of reduced-chlorophyll soybean mutants in field conditions. Front. Plant Sci., 2017, 8: 549 CrossRef
  87. Tyutereva E.V. Reaktsiya fotosinteticheskogo apparata chlorina 3613 (Hordeum vulgare L.), lishennogo khlorofilla b, na izmenenie urovnya insolyatsii. Avtoreferat kandidatskoi dissertatsii [Response of phorosynthetic apparatus of chlorina 3613 (Hordeum vulgare L.) deficient in chlorophyll b to altered insolation. PhD Thesis]. St. Petersburg, 2011 (in Russ.).
  88. Dmitrieva V.A., Ivanova A.N., Tyutereva E.V., Evkaikina A.I., Klimo-va E.A., Voitsekhovskaja O.V. Chlorophyllide-a-Oxygenase (CAO) deficiency affects the levels of singlet oxygen and formation of plasmodesmata in leaves and shoot apical meristems of barley. Plant Signaling & Behavior, 2017, 12(4): e1300732 CrossRef
  89. Leverenz J.W., Öquist G., Winglse G. Photosynthesis and photoinhibition in leaves of chlorophyll b-less barley in relation to absorbed light. Physiologia Plantarum, 1992, 85: 495-502 CrossRef
  90. Burch-Smith T.M., Zambryski P.C. Plasmodesmata paradigm shift: regulation from without versus within. Annu. Rev. Plant. Biol., 2012, 63: 239-260 CrossRef

 

back