Photosynthesis-Related Functions of Vasculature-Associated Chlorenchymatous Cells
In most biochemical, molecular, and genetic studies, a leaf is regarded as a uniformly responding unit, however leaves are not homogeneous in structure and function. Leaf venation is in continuity with the vascular system within leaf petiols and stems. Leaf veins are typically encircled by bundle sheath (BS) cells containing chloroplasts and photosynthetic cells adjacent to the vasculature are also found in petiols and stems. In C3 plants, BS cells have been shown to be preadapted for the role in C4 photosynthesis and this may explain the polyphyletic evolution of C4 photosynthesis. The photosynthetically active radiation (400–700 nm) reaching the chloroplast-containing cells adjacent to the vasculature in leaves, petiols, and stems is of lower intensity and enriched with longer wavelengths (~500–700 nm) when compared with that absorbed by mesophyll cells. The CO2 diffusion from the air to the vasculature-adjacent chlorenchymatous cells is also expected to be slow in comparison to mesophyll cells. However, the vasculature can be supplied with malate which releases CO2 after decarboxylation and with respiratory CO2 from heterotrophic tissues transported in the xylem. It could be expected that high CO2 concentration at the green cells around the vasculature supports carboxylation and photosynthesis. However, CO2-rich environment in stems impedes the photochemical activity of the photosynthetic vascular cells possibly through acidification of protoplasm and impairment of the pH-dependent excess energy quenching followed by reduction in the efficiency of heat dissipation. Light-dependent reduction in CO2 release, as shown in experiments on stems can predominantly be attributed to corticular refixation. All these can affect chloroplast ultrastructure, the composition of photosynthetic electron transport chain components, and the photosynthetic enzymatic machinery in these cells.
In BS cells, a higher heterotrophic/autotrophic ratio than in mesophyll cells causes a decrease in O2 level, intensity of photorespiration, and Mehler reaction. All these result in a decrease in PSII efficiency and stimulation of cyclic phosphorylation providing energetic support for the metabolism of BS cells.
One can conclude that vasculature-associated chlorenchymatous cells which are not able to fix atmospheric CO2 with the help of RubisCO can be supplied with carbon originating from β-carboxylating processes, which is reflected in the 13C discrimination value, and this process takes place in tissues growing at low light intensities enriched with longer wavelengths.
This work was supported by the Polish National Science Center (research grants N N304 156440 and 2011/01/B/NZ9/02540 and UMO-2016/21/B/NZ9/00813) and Alexander von Humboldt Foundation (AvH).
- van Bel AJE, Knoblauch M (2000) Sieve element and companion cell: the story of the comatose patient and the hyperactive nurse. Aust J Plant Physiol 27:477–487Google Scholar
- Burlat V, Oudin A, Courtois M, Rideau M, St-Pierre B (2004) Co-expression of three MEP pathway genes and geraniol 10-hydroxylase in internal phloem parenchyma of Catharanthus roseus implicates multicellular translocation of intermediates during the biosynthesis of monoterpene indole alkaloids and isoprenoid-derived primary metabolites. Plant J 38:131–141PubMedCrossRefGoogle Scholar
- Cernusak LA, Tcherkez G, Keitel C, Cornwell WK, Santiago LS, Knohl A, Barbour MM, Williams DG, Reich PB, Ellsworth DS, Dawson TE, Griffiths HG, Farquhar GD, Wright IJ (2009) Why are non-photosynthetic tissues generally 13C enriched compared with leaves in C3 plants? Review and synthesis of current hypotheses. Funct Plant Biol 36:199–213CrossRefGoogle Scholar
- Endo A, Sawada Y, Takahashi H, Okamoto M, Ikegami K, Koiwai H, Seo M, Toyomasu T, Mitsuhashi W, Shinozaki K, Nakazono M, Kamiya Y, Koshiba T, Nambara E (2008) Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiol 147:1984–1993PubMedPubMedCentralCrossRefGoogle Scholar
- Esau K (1977) Anatomy of seed plants, 2nd edn. Wiley, New YorkGoogle Scholar
- Galvez-Valdivieso G, Fryer MJ, Lawson T, Slattery K, Truman W, Smirnoff N, Asami T, Davies WJ, Jones AM, Baker NR, Mullineaux PM (2009) The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. Plant Cell 21:2143–2162PubMedPubMedCentralCrossRefGoogle Scholar
- Gorecka M, Alvarez-Fernandez R, Slattery K, McAusland L, DaveyPA KS, Lawson T, Mullineaux PM (2014) Abscisic acid signalling determines susceptibility of bundle sheath cells to photoinhibition in high light-exposed Arabidopsis leaves. Phil Trans R Soc B 369:20130234PubMedPubMedCentralCrossRefGoogle Scholar
- Haberlandt G (1914) Physiological Plant Anatomy (trans: Drummond M). Macmillan and Co., LondonGoogle Scholar
- Hofer MU, Santore UJ, Westhoff P (1992) Differential accumulation of the 10-,16- and 23-kDa peripheral components of the water-splitting complex of photosystem II in mesophyll and bundle sheath chloroplasts of the dicotyledonous C4 plant Flaveria trinervia (Spreng.) C.Mohr. Planta 186:304–312PubMedCrossRefGoogle Scholar
- Janacek SH, Trenkamp S, Palmer B, Brown NJ, Parsley K, Stanley S, Astley HM, Rolfe SA, Quick WP, Fernie AR, Hibberd JM (2009) Photosynthesis in cells around veins of the C3 plant Arabidopsis thaliana is important for both the shikimate pathway and leaf senescence as well as contributing to plant fitness. Plant J 59:329–343PubMedCrossRefGoogle Scholar
- Konieczny R, Banaś AK, Surówka E, Michalec Ż, Miszalski Z, Libik-Konieczny M (2014) Pattern of antioxidant enzyme activities and hydrogen peroxide content during developmental stages of rhizogenesis from hypocotyls explants of Mesembryanthemum crystallinum L. Plant Cell Rep 33:165–177PubMedCrossRefGoogle Scholar
- Kornas A, Miszalski Z, Surówka E, Fischer-Schliebs E, Lüttge U (2010a) Light stress is not effective to enhanced Crassulacean acid metabolism (CAM). Z Naturforsch 65c:79–86Google Scholar
- Kuźniak E, Kornas A, Kaźmierczak A, Rozpądek P, Nosek M, Kocurek M, Zellnig G, Müller M, Miszalski Z (2016) Photosynthesis-related characteristics of the midrib and the interveinal lamina in leaves of the C3–CAM intermediate plant Mesembryanthemum crystallinum. Ann Bot 117:1141–1151PubMedPubMedCentralCrossRefGoogle Scholar
- Lüttge U (2011) Photorespiration in phase III of Crassulacean acid metabolism: evolutionary and ecophysiological implications. Prog Bot 72:371–384Google Scholar
- Myburg AA, Sederoff RR (2001) Xylem structure and function. Nature Publishing Group. www.els.net
- Pilarski J, Tokarz K, Kocurek M (2008) Optical properties of the cork of stems and trunks of beech (Fagus sylvatica L.) Polish J Environ Stud 17:773–779Google Scholar
- Willis KJ, McElwain JC (2002) The evolution of plants. Oxford University Press, Oxford, UKGoogle Scholar