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      C 4-like photosynthesis and the effects of leaf senescence on C 4-like physiology in Sesuvium sesuvioides (Aizoaceae)

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          Abstract

          Sesuvium sesuvioides represents a young C 4 lineage with C 4-like metabolism: CO 2 compensation points range between C 4 and C 3–C 4 intermediate values, and Rubisco was detected in bundle sheath and mesophyll.

          Abstract

          Sesuvium sesuvioides (Sesuvioideae, Aizoaceae) is a perennial, salt-tolerant herb distributed in flats, depressions, or disturbed habitats of southern Africa and the Cape Verdes. Based on carbon isotope values, it is considered a C 4 species, despite a relatively high ratio of mesophyll to bundle sheath cells (2.7:1) in the portulacelloid leaf anatomy. Using leaf anatomy, immunocytochemistry, gas exchange measurements, and enzyme activity assays, we sought to identify the biochemical subtype of C 4 photosynthesis used by S. sesuvioides and to explore the anatomical, physiological, and biochemical traits of young, mature, and senescing leaves, with the aim to elucidate the plasticity and possible limitations of the photosynthetic efficiency in this species. Assays indicated that S. sesuvioides employs the NADP-malic enzyme as the major decarboxylating enzyme. The activity of C 4 enzymes, however, declined as leaves aged, and the proportion of water storage tissue increased while air space decreased. These changes suggest a functional shift from photosynthesis to water storage in older leaves. Interestingly, S. sesuvioides demonstrated CO 2 compensation points ranging between C 4 and C 3–C 4 intermediate values, and immunocytochemistry revealed labeling of the Rubisco large subunit in mesophyll cells. We hypothesize that S. sesuvioides represents a young C 4 lineage with C 4-like photosynthesis in which C 3 and C 4 cycles are running simultaneously in the mesophyll.

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          Most cited references 51

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          The evolution of C4photosynthesis

           Rowan Sage (2004)
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            C4 photosynthesis: a unique elend of modified biochemistry, anatomy and ultrastructure

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              Kranz anatomy is not essential for terrestrial C4 plant photosynthesis.

              An important adaptation to CO2-limited photosynthesis in cyanobacteria, algae and some plants was development of CO2-concentrating mechanisms (CCM). Evolution of a CCM occurred many times in flowering plants, beginning at least 15-20 million years ago, in response to atmospheric CO2 reduction, climate change, geological trends, and evolutionary diversification of species. In plants, this is achieved through a biochemical inorganic carbon pump called C4 photosynthesis, discovered 35 years ago. C4 photosynthesis is advantageous when limitations on carbon acquisition are imposed by high temperature, drought and saline conditions. It has been thought that a specialized leaf anatomy, composed of two, distinctive photosynthetic cell types (Kranz anatomy), is required for C4 photosynthesis. We provide evidence that C4 photosynthesis can function within a single photosynthetic cell in terrestrial plants. Borszczowia aralocaspica (Chenopodiaceae) has the photosynthetic features of C4 plants, yet lacks Kranz anatomy. This species accomplishes C4 photosynthesis through spatial compartmentation of photosynthetic enzymes, and by separation of two types of chloroplasts and other organelles in distinct positions within the chlorenchyma cell cytoplasm.
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                Author and article information

                Journal
                J Exp Bot
                J. Exp. Bot
                exbotj
                Journal of Experimental Botany
                Oxford University Press (UK )
                0022-0957
                1460-2431
                15 February 2019
                24 January 2019
                24 January 2019
                : 70
                : 5
                : 1553-1565
                Affiliations
                [1 ]Institut für Molekulare Physiologie, Johannes Gutenberg-Universität, Mainz, Germany
                [2 ]Institut für Organismische und Molekulare Evolutionsbiologie, Johannes Gutenberg-Universität, Mainz, Germany
                [3 ]Philipps-Universität, FB 16–Pharmazie, Marburg, Germany
                [4 ]Max Planck Institute for Chemistry, Multiphase Chemistry Department, Mainz, Germany
                [5 ]School of Molecular Sciences [310], University of Western Australia, Crawley, Western Australia, Australia
                Author notes
                Article
                erz011
                10.1093/jxb/erz011
                6411375
                30689935
                © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Experimental Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Pages: 13
                Product
                Funding
                Funded by: Sybille Kalkhof-Rose Foundation
                Award ID: KA1816-7-1
                Funded by: German Science Foundation
                Categories
                Research Papers
                Photosynthesis and Metabolism

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