Light-Dependent Reactions of Photosynthesis in Mesophyll and Bundle Sheath Chloroplasts of C4 Plant Maize. How Our Views Have Changed in Recent Years

Elżbieta Romanowska, Wioleta Wasilewska-Dębowska

Abstract


Plants experience a range of light intensities and qualities in their environment. Leaves are subjected to spatial and temporal gradients in incident light, which has major consequences in the photosynthetic carbon assimilation. Plants acclimate to light by developing a range of mechanisms, from adjustments in leaf morphology to changes in the photosynthetic apparatus stoichiometry. In C4 plants, light intensity is a major limiting factor for photosynthesis at optimum temperatures. Under limiting light, it is not clear if all of factors (e.g., temperature, mineral nutrition, water supply) are co-limiting or if there is one primary limitation. Differences in light quality and intensity have a profound impact on C4 photosynthesis, where pathways require metabolic coordination of the mesophyll and bundle sheath cycles. Changes in the linear versus cyclic electron flux in maize (NADP-malic enzyme C4 subtype) in the mesophyll and bundle sheath chloroplasts in response to light may lead to an imbalance in the coordination of the C3 and C4 pathways. Additionally, the rearrangement of the thylakoid complexes of both types of chloroplasts in maize optimizes the light energy distribution between the mesophyll and bundle sheath cells and may also participate in energy dissipation. This review aims to highlight the changes in the understanding of the functions of photosystem II in maize bundle sheath chloroplasts and the role of super and megacomplexes in the thylakoids.

Keywords


C4 plants; light reaction of photosynthesis; maize; mesophyll and bundle sheath thylakoids; photosystem II

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References


Aguilera, Y., Herrera, T., Liébana, R., Rebollo-Hernanz, M., Sanchez-Puelles, C., & Martín-Cabrejas, M. A. (2015). Impact of melatonin enrichment during germination of legumes on bioactive compounds and antioxidant activity. Journal of Agricultural and Food Chemistry, 63(36), 7967–7974. https://doi.org/10.1021/acs.jafc.5b03128

Allakhverdiev, S. I., & Murata, N. (2004). Environmental stress inhibits the synthesis de novo of D1 protein in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochimica et Biophysica Acta, 1657(1), 23–32. https://doi.org/10.1016/j.bbabio.2004.03.003

Allen, J. F. (1992). Protein phosphorylation in regulation of photosynthesis. Biochimica et Biophysica Acta, 1098(3), 275–335. https://doi.org/10.1016/s0005-2728(09)91014-3

Allen, J. F. (2002). Plastoquinone redox control of chloroplast thylakoid protein phosphorylation and distribution of excitation energy between photosystems: Discovery, background, implications. Photosynthesis Research, 73(1–3), 139–148. https://doi.org/10.1023/A:1020414106993

Allen, J. F. (2004). Cytochrome b6f: Structure for signalling and vectorial metabolism. Trends in Plant Science, 9(3), 130–137. https://doi.org/10.1016/j.tplants.2004.01.009

Allen, J. F., Bennett, J., Steinback, K. E., & Arntzen, C. J. (1981). Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature, 291, 25–29. https://doi.org/10.1038/291025a0

Andersson, B., & Aro, E. M. (2001). Photodamage and D1 protein turnover in photosystem II. In B. Andersson & E. M. Aro (Eds.), Regulation of photosynthesis (pp. 377–393). Kluwer Academic Publishers. https://doi.org/10.1007/0-306-48148-0_22

Atkin, O. K., Millar, A. H., Gardeström, P., & Day, D. A. (2000). Photosynthesis, carbohydrate metabolism and respiration in leaves of higher plants. In R. C. Leegood, T. D. Sharkey, & S. von Caemmerer (Eds.), Photosynthesis, physiology and metabolism (pp. 153–175). Kluwer Academic Publishers. https://doi.org/10.1007/0-306-48137-5_7

Bailey, S., Walters, R. G., Jansson, S., & Horton, P. (2001). Acclimation of Arabidopsis thaliana to the light environment: The existence of separate low light and high light responses. Planta, 213(5), 794–801. https://doi.org/10.1007/s004250100556

Bassi, R., Marquardt, J., & Lavergne, J. (1995). Biochemical and functional properties of photosystem II in agranal membranes from maize mesophyll and bundle sheath chloroplasts. European Journal of Biochemistry, 233(3), 709–719. https://doi.org/10.1111/j.1432-1033.1995.709_3.x

Bassi, R., & Passera, C. (1982). Effect of growth conditions on carboxylating enzymes of Zea mays plants. Photosynthesis Research, 3(1), 53–58. https://doi.org/10.1007/BF00030049

Bazzaz, M. B., & Govindjee, (1973). Photochemical properties of mesophyll and bundle sheath chloroplasts of maize. Plant Physiology, 52(3), 257–262. https://doi.org/10.1104/pp.52.3.257

Bellasio, C., & Griffiths, H. (2014). The operation of two decarboxylases, transamination, and partitioning of C4 metabolic processes between mesophyll and bundle sheath cells allows light capture to be balanced for the maize C4 pathway. Plant Physiology, 164(1), 466–480. https://doi.org/10.1104/pp.113.228221

Bennett, J. (1977). Phosphorylation of chloroplast membrane polypeptides. Nature, 269, 344–346. https://doi.org/10.1038/269344a0

Bonente, G., Howes, B. D., Caffarri, S., Smulevich, G., & Bassi, R. (2008). Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro. Journal of Biological Chemistry, 283(13), 8434–8445. https://doi.org/10.1074/jbc.M708291200

Botha, C. E. J. (1992). Plasmodesmatal distribution, structure and frequency in relation to assimilation in C3 and C4 grasses in southern Africa. Planta, 187(3), 348–358. https://doi.org/10.1007/BF00195658

Botha, C. E. J., & Evert, R. F. (1988). Plasmodesmatal distribution and frequency in vascular bundles and contiguous tissues of the leaf of Themeda triandra. Planta, 173(4), 433–441. https://doi.org/10.1007/BF00958954

Bräutigam, A., Schliesky, S., Külahoglu, C., Osborne, C. P., & Weber, A. P. M. (2014). Towards an integrative model of C4 photosynthetic subtypes: Insights from comparative transcriptome analysis of NAD-ME, NADP-ME, and PEP-CK C4 species. Journal of Experimental Botany, 6(13), 3579–3593. https://doi.org/10.1093/jxb/eru100

Broglie, R., Coruzzi, G., Keith, B., & Chua, N. H. (1984). Molecular biology of C4 photosynthesis in Zea mays: Differential localization of proteins and mRNA in the two leaf cell types. Plant Molecular Biology, 3(6), 431–444. https://doi.org/10.1007/BF00033391

Buchman, N., Brooks, J. R., Rapp, K. D., & Ehleringer, J. R. (1996). Carbon isotope composition of C4 grasses is influenced by light and water supply. Plant, Cell & Environment, 19(4), 392–402. https://doi.org/10.1111/j.1365-3040.1996.tb00331.x

Chapman, K. S. R., Berry, J. A., & Hatch, M. D. (1980). Photosynthetic metabolism in bundle sheath cells of the C4 species Zea mays: Source of ATP and NADPH and the contribution of Photosystem II. Archives of Biochemistry and Biophysics, 202(2), 330–341. https://doi.org/10.1016/0003-9861(80)90435-x

Chapman, K. S. R., & Hatch, M. D. (1981). Aspartate decarboxylation in bundle sheath cells of Zea mays and its possible contribution to C4 photosynthesis. Australian Journal of Plant Physiology, 8(2), 237–248. https://doi.org/10.1071/PP9810237

Covshoff, S., Majeran, W., Liu, P., Kolkman, J. M., van Wijk, K. J., & Brutnell, T. P. (2008). Deregulation of maize C4 photosynthetic development in a mesophyll cell-defective mutant. Plant Physiology, 146(4), 1469–1481. https://doi.org/10.1104/pp.107.113423

Danila, F. R., Quick, W. P., White, R. G., Furbank, R. T., & von Caemmerer, S. (2016). The metabolite pathway between bundle sheath and mesophyll: Quantification of plasmodesmata in leaves of C3 and C4 monocots. The Plant Cell, 28(6), 1461–1471. https://doi.org/10.1105/tpc.16.00155

Darie, C. C., de Pascalis, L., Mutschler, B., & Haehnel, W. (2006). Studies of the Ndh complex and photosystem II from mesophyll and bundle sheath chloroplasts of the C4-type plant Zea mays. Journal of Plant Physiology, 163(8), 800–808. https://doi.org/10.1016/j.jplph.2005.11.014

Downton, W. J. S., & Pyliotis, N. A. (1971). Loss of photosystem II during ontogeny of sorghum bundle sheath chloroplasts. Canadian Journal of Botany, 49(1), 179–180. https://doi.org/10.1139/b71-030

Drożak, A., & Romanowska, E. (2006). Acclimation of mesophyll and bundle sheath chloroplasts of maize to different irradiances during growth. Biochimica et Biophysica Acta, 1757(11), 1539–1546. https://doi.org/10.1016/j.bbabio.2006.09.001

Ebbert, V., & Godde, D. (1996). Phosphorylation of PSII polypeptides inhibits D1 protein degradation and increases PSII stability. Photosynthesis Research, 50(3), 257–269. https://doi.org/10.1007/BF00033124

Edwards, G. E., Franceschi, V. R., Ku, M. S. B., Voznesenskaya, E. V., Pyankov, V. I., & Andreo, C. S. (2001). Compartmentation of photosynthesis in cell and tissues of C4 plants. Journal of Experimental Botany, 52(356), 577–590. https://doi.org/10.1093/jxb/52.356.577

Edwards, G. E., & Huber, S. C. (1981). The C4 pathway. In M. D. Hatch & N. K. Boardman (Eds.), The biochemistry of plants. A comprehensive treatise (pp. 237–280). Academic Press. https://doi.org/10.1016/B978-0-12-675408-7.50012-4

Edwards, G. E., McC. Lilley, R., Craig, S., & Hatch, M. D. (1979). Isolation of intact and functional chloroplasts from mesophyll and bundle sheath protoplasts of the C4 plant Panicum miliaceum. Plant Physiology, 63(5), 821–827. https://doi.org/10.1104/pp.63.5.821

Edwards, G. E., & Walker, D. A. (1983). C3, C4: Mechanisms, and cellular and environmental regulation, of photosynthesis. Blackwell Scientific Publications.

Evans, J. R., & Vogelmann, T. C. (2003). Profiles of 14 C fixation through spinach leaves in relation to light absorption and photosynthetic capacity. Plant, Cell & Environment, 26(4), 547–560. https://doi.org/10.1046/j.1365-3040.2003.00985.x

Evans, J. R., Vogelmann, T. C., & von Caemmerer, S. (2007). Balancing light capture with distributed metabolic demand during C4 photosynthesis. In J. E. Sheehy, P. L. Mitchell, & B. Hardy (Eds.), Charting new pathways to C4 rice (pp. 127–143). World Scientific Publishing. https://doi.org/https://doi.org/10.1142/9789812709523_0008

Evert, R. F., Eschrich, W., & Heyser, W. (1977). Distribution and structure of the plasmodesmata in mesophyll and bundle sheath cells of Zea mays L. Planta, 136, 77–89. https://doi.org/10.1007/BF00387929

Evert, R. F., Eschrich, W., & Heyser, W. (1978). Leaf structure in relation to solute transport and phloem loading in Zea mays L. Planta, 138(3), 70–89. https://doi.org/10.1007/BF00386823

Flexas, J., Escalona, J. M., & Medrano, H. (1998). Down-regulation of photosynthesis by drought under field conditions in grapevine leaves. Functional Plant Biology, 25(8), 893–900. https://doi.org/10.1071/PP98054

Fristedt, R., Wasilewska, W., Romanowska, E., & Vener, A. V. (2012). Differential phosphorylation of thylakoid proteins in mesophyll and bundle sheath chloroplasts from maize plants grown under low or high light. Proteomics, 12(18), 2852–2861. https://doi.org/10.1002/pmic.201200196

Furbank, R. T. (2011). Evolution of the C4 photosynthetic mechanism: Are there really three C4 acid decarboxylation types? Journal of Experimental Botany, 62(9), 3103–3108. https://doi.org/10.1093/jxb/err080

Ghirardi, M. L., & Melis, A. (1983). Localization of photosynthetic electron transport components in mesophyll and bundle sheath chloroplasts of Zea mays. Archives of Biochemistry and Biophysics, 224(1), 19–28. https://doi.org/10.1016/0003-9861(83)90186-8

Grieco, M., Suorsa, M., Jajoo, A., Tikkanen, M., & Aro, E. M. (2015). Light harvesting II antenna trimers connect energetically the entire photosynthetic machinery – Including both photosystems II and I. Biochimica et Biophysica Acta – Bioenergetics, 1847(6–7), 607–619. https://doi.org/10.1016/j.bbabio.2015.03.004

Hardt, H., & Kok, B. (1978). Comparison of the photosynthetic activities of spinach chloroplasts with those of corn mesophyll and corn bundle sheath tissue. Plant Physiology, 62(1), 59–63. https://doi.org/10.1104/pp.62.1.59

Hatch, M. D. (1987). C4 photosynthesis: A unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta – Reviews on Bioenergetics, 895(2), 81–106. https://doi.org/10.1016/S0304-4173(87)80009-5

Hatch, M. D. (1992). C4 photosynthesis: An unlikely process full of surprises. Plant Cell Physiology, 33(4), 333–342. https://doi.org/10.1093/oxfordjournals.pcp.a078260

Hatch, M. D. (1999). C4 photosynthesis: A historical overview. In R. F. Sage & R. K. Monson (Eds.), C4 plant biology (pp. 17–46). Academic Press. https://doi.org/10.1016/B978-012614440-6/50003-3

Hatch, M. D. (2002). C4 photosynthesis: Discovery and resolution. Photosynthesis Research, 73, Article 251. https://doi.org/10.1023/A:1020471718805

Haussühl, K., Andersson, B., & Adamska, I. (2001). A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. EMBO Journal, 20(4), 713–722. https://doi.org/10.1093/emboj/20.4.713

Itzhaki, H., Naveh, L., Lindahl, M., Cook, M., & Adam, Z. (1998). Identification and characterization of DegP, a serine protease associated with the luminal side of the thylakoid membrane. Journal of Biological Chemistry, 27(12), 7094–7098. https://doi.org/10.1074/jbc.273.12.7094

Ivanov, B. N., Asada, K., Kramer, D. M., & Edwards, G. (2005). Characterization of photosynthetic electron transport in bundle sheath cells of maize. Ascorbate effectively stimulates cyclic electron flow around PSI. Planta, 220(4), 572–581. https://doi.org/10.1007/s00425-004-1367-6

Ivanov, B., Asada, K., & Edwards, G. E. (2007). Analysis of donors of electrons to photosystem I and cyclic electron flow by redox kinetics of P700 in chloroplasts of isolated bundle sheath strands of maize. Photosynthesis Research, 92(1), 65–74. https://doi.org/10.1007/s11120-007-9166-0

Kargul, J., & Barber, J. (2008). Photosynthetic acclimation structural reorganization of light harvesting antenna – Role of redox-dependent phosphorylation of major and minor chlorophyll a/b binding proteins. FEBS Journal, 275(6), 1056–1068. https://doi.org/10.1111/j.1742-4658.2008.06262.x

Ketchner, S. L., & Sayre, R. T. (1992). Characterization of the expression of the photosystem II–Oxygen evolution complex in C4 species of Flaveria. Plant Physiology, 98(3), 1154–1162. https://doi.org/10.1104/pp.98.3.1154

Kono, M., & Terashima, I. (2014). Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. Journal of Photochemistry and Photobiology B: Biology, 137, 89–99. https://doi.org/10.1016/j.jphotobiol.2014.02.016

Kono, M., & Terashima, I. (2016). Elucidation of photoprotective mechanisms of PSI against fluctuating light photoinhibition. Plant Cell Physiology, 57(7), 1405–1414. https://doi.org/10.1093/pcp/pcw103

Krömer, S. (1995). Respiration during photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology, 46, 45–70. https://doi.org/10.1146/annurev.pp.46.060195.000401

Ku, S. B., Gutierrez, M., Kanai, R., & Edwards, G. E. (1974). Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types of C4 plants II. Chlorophyll and hill reaction studies. Zeitschriftfür Pflanzenphysiologie, 72(4), 320–337. https://doi.org/10.1016/S0044-328X(74)80073-5

Laetsch, W. M. (1971). Chloroplast structural relationships in leaves of C4 plants. In M. D. Hatch, C. B. Osmond, & R. O. Slayter (Eds.), Photosynthesis and photorespiration (pp. 323–349). Wiley-Interscience.

Laisk, A., Vello, O., Eichelmann, H., & Dall’Osto, L. (2014). Action spectra of photosystems II and I and quantum yield of photosynthesis in leaves in State 1. Biochimica et Biophysica Acta, 1837(2), 315–325. https://doi.org/10.1016/j.bbabio.2013.12.001

Langdale, J. A., Zelitch, I., Miller, E., & Nelson, T. (1988). Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. EMBO Journal, 7(12), 3643–3651. https://doi.org/10.1002/j.1460-2075.1988.tb03245.x

Leegood, R. C. (2000). Transport during C4 photosynthesis. In R. C. Leegood, T. D. Sharkey, & S. von Caemmerer (Eds.), Photosynthesis: Physiology and metabolism (pp. 459–469). Kluwer. https://doi.org/10.1007/0-306-48137-5_19

Leegood, R. C., Crowther, D., & Walker, D. A. (1981). Photosynthetic electron transport in the bundle sheath of maize. FEBS Letters, 126(1), 89–92. https://doi.org/10.1016/0014-5793(81)81040-X

Leegood, R. C., Crowther, D., Walker, D. A., & Hind, G. (1983). Energetics of photosynthesis in Zea mays. I. Studies of the flash-induced electrochromic shift and fluorescence induction in bundle sheath cells. Biochimica et Biophysica Acta – Bioenergetics, 722(1), 116–126. https://doi.org/10.1016/0005-2728(83)90164-0

Leegood, R. C., & Walker, R. P. (1999). Regulation of the C4 pathway. In R. F. Sage & R. K. Monson (Eds.), C4 plant biology (pp. 89–131). Academic Press. https://doi.org/10.1016/B978-012614440-6/50005-7

Lindahl, M., Spetea, C., Hundal, T., Oppenheim, A. B., Adam, Z., & Andersson, B. (2000). The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. Plant Cell, 12(3), 419–431. https://doi.org/10.1105/tpc.12.3.419

Long, S. P., Farage, P. K., & Rohrhofer, U. (1989). Separating the contribution of the upper and lower mesophyll to photosynthesis in Zea mays L. leaves. Planta, 177(2), 207–216. https://doi.org/10.1007/BF00392809

Loreto, F., Tsonev, T., & Centritto, M. (2009). The impact of blue light on leaf mesophyll conductance. Journal of Experimental Botany, 60(8), 2283–2290. https://doi.org/10.1093/jxb/erp112

Lu, Y.-K., & Stemler, A. J. (2002). Extrinsic photosystem II carbonic anhydrase in maize mesophyll chloroplasts. Plant Physiology, 128(2), 643–649. https://doi.org/10.1104/pp.010643

Ludwig, M. (2016). The roles of organic acids in C4 photosynthesis. Frontiers in Plant Science, 7, Article 647. https://doi.org/10.3389/fpls.2016.00647

Mayne, B. C., Dee, A. M., & Edwards, G. E. (1974). Photosynthesis in mesophyll protoplasts and bundle sheath cells of various type of C4 plants. III. Fluorescence emission spectra, delayed light emission, and P700 content. Zeitschriftfür Pflanzenphysiologie, 74(4), 275–291. https://doi.org/10.1016/S0044-328X(75)80158-9

Meierhoff, K., & Westhoff, P. (1993). Differential biogenesis of photosystem II in mesophyll and bundle sheath cells of monocotyledonous NADP malic enzyme-type C4 plants: The non-stoichiometric abundance of the subunits of photosystem II in the bundle sheath chloroplasts and the translational activity of the plastome-encoded genes. Planta, 191, 13–33. https://doi.org/10.1007/BF00240892

Meister, M., Agostino, A., & Hatch, M. D. (1996). The roles of malate and aspartate in C4 photosynthetic metabolism of Flaveria bidentis (L.). Planta, 199, 262–269. https://doi.org/10.1007/BF00196567

Munekage, Y. N., & Taniguchi, Y. Y. (2016). Promotion of cyclic electron transport around photosystem I with the development of C4 photosynthesis. Plant and Cell Physiology, 57(5), 897–903. https://doi.org/10.1093/pcp/pcw012

Nelson, T., & Langdale, J. A. (1989). Patterns of leaf development in C4 plants. The Plant Cell, 1(1), 3–13. https://doi.org/10.1105/tpc.1.1.3

Osborne, C. P., & Sack, L. (2012). Evolution of C4 plants: A new hypothesis for an interaction of CO2 and water relations mediated by plant hydraulics. Philosophical Transactions of the Royal Society B, 367(1588), 583–600. https://doi.org/10.1098/rstb.2011.0261

Parys, E., & Jastrzębski, H. (2006). Light-enhanced dark respiration in leaves, isolated cells and protoplasts of various types of C4 plants. Journal of Plant Physiology, 163(6), 638–647. https://doi.org/10.1016/j.jplph.2005.05.009

Pesaresi, P., Pribil, M., Wunder, T., & Leister, D. (2011). Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: The roles of STN7, STN8 and TAP38. Biochimica et Biophysica Acta, 1807(8), 887–896. https://doi.org/10.1016/j.bbabio.2010.08.002

Pfündel, E., Nagel, E., & Meister, A. (1996). Analyzing the light energy distribution in the photosynthetic apparatus of C4 plants using highly purified mesophyll and bundle sheath thylakoids. Plant Physiology, 112(3), 1055–1070. https://doi.org/10.1104/pp.112.3.1055

Pokorska, B., & Romanowska, E. (2007). Photoinhibition and D1 protein degradation in mesophyll and agranal bundle sheath thylakoids of maize. Functional Plant Biology, 34(9), 844–852. https://doi.org/10.1071/FP07067

Pokorska, B., Zienkiewicz, M., Powikrowska, M., Drozak, A., & Romanowska, E. (2009). Differential turnover of the photosystem II reaction centre D1 protein in mesophyll and bundle sheath chloroplasts of maize. Biochimica et Biophysica Acta, 1787(10), 1161–1169. https://doi.org/10.1016/j.bbabio.2009.05.002

Polya, G. M., & Osmond, C. B. (1972). Phosphorylation by mesophyll and bundle sheath chloroplasts of C4 plants. Plant Physiology, 49(2), 267–269. https://doi.org/10.1104/pp.49.2.267

Rao, X., & Dixon, R. A. (2016). The differences between NAD-ME and NADP-ME subtypes of C4 photosynthesis: More than decarboxylating enzymes. Frontiers in Plant Science, 7, Article 1525. https://doi.org/10.3389/fpls.2016.01525

Rao, X., Lu, N., Li, G., Nakashima, J., Tang, Y., & Dixon, R. A. (2016). Comparative cell-specific transcriptomics reveals differentiation of C4 photosynthesis pathways in switchgrass and other C4 lineages. Journal of Experimental Botany, 67, 1649–1662. https://doi.org/10.1093/jxb/erv553

Rintämaki, E., Kettunen, R., & Aro, E. M. (1996). Differential D1 dephosphorylation in functional and photodamaged photosystem II centers. Journal of Biological Chemistry, 271(25), 14870–14875. https://doi.org/10.1074/jbc.271.25.14870

Rintämaki, E., Salo, R., Koivuniemi, A., & Aro, E. M. (1996). Protein phosphorylation and magnesium status regulate the degradation of the D1 reaction centre protein of photosystem II. Plant Science, 115(2), 175–182. https://doi.org/10.1016/0168-9452(96)04343-9

Rogowski, P., Wasilewska-Dębowska, W., Krupnik, T., Drożak, A., Zienkiewicz, M., Krysiak, M., & Romanowska, E. (2019). Photosynthesis and organization of maize mesophyll and bundle sheath thylakoids of plants grown in various light intensities. Environmental and Experimental Botany, 162, 72–86. https://doi.org/10.1016/j.envexpbot.2019.02.006

Rogowski, P., Wasilewska-Dębowska, W., Urban, A., & Romanowska, E. (2018). Maize bundle sheath chloroplasts – A unique model of permanent State 2. Environmental and Experimental Botany, 155, 321–331. https://doi.org/10.1016/j.envexpbot.2018.07.012

Romanowska, E., Buczyńska, A., Wasilewska, W., Krupnik, T., Drożak, A., Rogowski, P., Parys, E., & Zienkiewicz, M. (2017). Differences in photosynthetic responses of NADP-ME type C4 species to high light. Planta, 245(3), 641–657. https://doi.org/10.1007/s00425-016-2632-1

Romanowska, E., & Drożak, A. (2006). Comparative analysis of biochemical properties of mesophyll and bundle sheath chloroplasts from various subtypes of C4 plants grown at moderate irradiance. Acta Biochimica Polonica, 53(4), 709–719. https://doi.org/10.18388/abp.2006_3298

Romanowska, E., Drożak, A., Pokorska, B., Shiell, B. J., & Michalski, W. P. (2006). Organization and activity of photosystems from the mesophyll and bundle sheath chloroplasts of maize. Journal of Plant Physiology, 163(6), 607–618. https://doi.org/10.1016/j.jplph.2005.06.007

Romanowska, E., Drożak, A., Powikrowska, M., Zienkiewicz, M., & Pokorska, B. (2008). Mechanisms of photosynthetic apparatus acclimation of C4 plants to different irradiances. In J. F. Allen, E. Gantt, J. H. Goldbeck, & B. Osmond (Eds.), Photosynthesis. Energy from the sun (pp. 1039–1042). Springer. https://doi.org/10.1007/978-1-4020-6709-9_227

Romanowska, E., Kargul, J., Powikrowska, M., Finazzi, G., Nield, J., Drożak, A., & Pokorska, B. (2008). Structural organization of photosynthetic apparatus in agranal chloroplasts of maize. Journal of Biological Chemistry, 283(38), 26037–26046. https://doi.org/10.1074/jbc.M803711200

Romanowska, E., Powikrowska, M., Zienkiewicz, M., Drożak, A., & Pokorska, B. (2008). High light induced accumulation of two isoforms of the CF1 α-subunit in mesophyll and bundle sheath chloroplasts of C4 plants. Acta Biochimica Polonica, 55, 175–182. https://doi.org/10.18388/abp.2008_3110

Ruban, A. V. (2015). Evolution under the sun: Optimizing light harvesting in photosynthesis. Journal of Experimental Botany, 66(1), 7–23. https://doi.org/10.1093/jxb/eru400

Schuster, G., Ohad, I., Martineau, B., & Taylor, W. C. (1985). Differentiation and development of bundle sheath and mesophyll thylakoids in maize. Thylakoid polypeptide composition, phosphorylation, and organization of photosystem II. Journal of Biological Chemistry, 260(21), 11866–11873. https://doi.org/10.1016/S0021-9258(17)39111-1

Schwarz, E. M., Tietz, S., & Froehlich, J. (2018). Photosystem I-LHCII megacomplexes respond to high light and aging in plants. Photosynthesis Research, 136(1), 107–124. https://doi.org/10.1007/s11120-017-0447-y

Sheen, J. Y., & Bogorad, L. (1987). Regulation of levels of nuclear transcripts for C4 photosynthesis in bundle sheath and mesophyll cells of maize leaves. Plant Molecular Biology, 8(3), 227–238. https://doi.org/10.1007/BF00015031

Sowiński, P. (1998). The effect of irradiance, p-chloromercuribenzenesulphonic acid and fusicoccin on the long distance transport in Zea mays L. seedlings. Acta Physiologiae Plantarum, 20, 79–84. https://doi.org/10.1007/s11738-998-0047-8

Sowiński, P., Bilska, A., Barańska, K., Fronk, J., & Kobus, P. (2007). Plasmodesmata density in vascular bundles in leaves of C4 grasses grown at different light conditions in respect to photosynthesis and photosynthate export efficiency. Environmental and Experimental Botany, 61(1), 74–84. https://doi.org/10.1016/j.envexpbot.2007.03.002

Takabayashi, A., Kishine, M., Asada, K., Endo, T., & Sato, F. (2005). Differential use of two cyclic electron flows around photosystem I for driving CO2 -concentration mechanism in C4 photosynthesis. Proceedings of the National Academy of Sciences of the United States of America, 102(46), 16898–16903. https://doi.org/10.1073/pnas.0507095102

Terashima, I., Sakaguchi, S., & Hara, N. (1986). Intra-leaf and intra cellular gradients in chloroplast ultrastructure of dorsiventral leaves illuminated from the adaxial or abaxial side during their development. Plant and Cell Physiology, 27(6), 1023–1031. https://doi.org/10.1093/oxfordjournals.pcp.a077185

Tikkanen, M., Grieco, M., Kangasjärvi, S., & Aro, E. M. (2010). Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiology, 152(2), 723–735. https://doi.org/10.1104/pp.109.150250

Tikkanen, M., Piippo, M., Suorsa, M., Sirpiö, S., Mulo, P., Vainonen, J., Vener, A. V., Allahverdiyeva, J., & Aro, E. M. (2006). State transitions revisited – A buffering system for dynamic low light acclimation of Arabidopsis. Plant Molecular Biology, 62(4–5), 779–793. https://doi.org/10.1007/s11103-006-9044-8

Ueno, O., Yoshimura, Y., & Sentoku, N. (2005). Variation in the activity of some enzymes of photorespiratory metabolism in C4 grasses. Annals of Botany, 96(5), 863–869. https://doi.org/10.1093/aob/mci238

Urban, A., Rogowski, P., Wasilewska-Dębowska, W., & Romanowska, E. (2020). Effect of light on the rearrangements of PSI super- and megacomplexes in the non-appressed thylakoid domains of maize mesophyll chloroplasts. Plant Science, 301, Article 110655. https://doi.org/10.1016/j.plantsci.2020.110655

Usuda, H., Kanai, R., & Miyachi, S. (1975). Carbon dioxide assimilation and photosystem II deficiency in bundle sheath strands isolated from C4 plants. Plant and Cell Physiology, 16(3), 485–494. https://doi.org/10.1093/oxfordjournals.pcp.a075164

Vainstein, A., Ferreira, P., Peterson, C. C., Verbeke, J. A., & Thornber, J. P. (1989). Expression of the major light-harvesting chlorophyll a/b-protein and its import into thylakoids of mesophyll and bundle sheath chloroplasts of maize. Plant Physiology, 89(2), 602–609. https://doi.org/10.1104/pp.89.2.602

Vialet-Chabrand, S., Matthews, J. S. A., Simkin, A. J., Raines, C. A., & Lawson, T. (2017). Importance of fluctuations in light on plant photosynthetic acclimation. Plant Physiology, 173(4), 2163–2179. https://doi.org/10.1104/pp.16.01767

von Caemmerer, S., & Furbank, R. T. (1999). Modeling C4 photosynthesis. In R. F. Sage & R. K. Monson (Eds.), C4 plant biology (pp. 173–211). Academic Press. https://doi.org/10.1016/B978-012614440-6/50007-0

von Caemmerer, S., & Furbank, R. T. (2003). The C4 pathway: An efficient CO2 pump. Photosynthesis Research, 77(2–3), Article 191. https://doi.org/10.1023/A:1025830019591

Voznesenskaya, E. V., Franceschi, V. R., Chuong, S. D. X., & Edwards, G. E. (2006). Functional characterization of phosphoenolpyruvate carboxykinase-type C4 leaf anatomy: Immuno-, cytochemical and ultrastructural analyses. Annals of Botany, 98(1), 77–91. https://doi.org/10.1093/aob/mcl096

Walker, G. H., & Izawa, S. (1979). Photosynthetic electron transport in isolated maize bundle sheath cells. Plant Physiology, 63(1), 133–138. https://doi.org/10.1104/pp.63.1.133

Walters, R. W. (2005). Towards an understanding of photosynthetic acclimation. Journal of Experimental Botany, 56(411), 435–447. https://doi.org/10.1093/jxb/eri060

Wang, C., Guo, L., Li, Y., & Wang, Z. (2012). Systematic comparison of C3 and C4 plants based on metabolic network analysis. BMC Systems Biology, 6(Suppl. 2), Article S9. https://doi.org/10.1186/1752-0509-6-S2-S9

Wollman, F. A. (2001). State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO Journal, 20, 3623–3630. https://doi.org/10.1093/emboj/20.14.3623

Woo, K. C., Anderson, J. M., Boardman, N. K., Downton, W. J. S., Osmond, C. B., & Thorne, S. W. (1970). Deficient photosystem II in agranal bundle sheath chloroplasts of C4 plants. Proceedings of the National Academy of Sciences of the United States of America, 67(1), 18–25. https://doi.org/10.1073/pnas.67.1.18

Zienkiewicz, M., Drożak, A., Wasilewska, W., Bacławska, I., Przedpełska-Wąsowicz, E., & Romanowska, E. (2015). The short-term response of Arabidopsis thaliana (C3) and Zea mays (C4) chloroplasts to red and far red light. Planta, 242(6), 1479–1493. https://doi.org/10.1007/s00425-015-2392-3

Zienkiewicz, M., Ferenc, A., Wasilewska, W., & Romanowska, E. (2012). High light stimulates Deg1-dependent cleavage of the minor LHCII antenna proteins CP26 and CP29 and the PsbS protein in Arabidopsis thaliana. Planta, 235, 279–288. https://doi.org/10.1007/s00425-011-1505-x




DOI: https://doi.org/10.5586/asbp.9112

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