Flowers of Bienertia cycloptera and Suaeda aralocaspica (Chenopodiaceae) complete the life cycle performing single-cell C4 photosynthesis
Christine N. Boyd A , Vincent R. Franceschi A , Simon D. X. Chuong A B , Hossein Akhani C , Olavi Kiirats A , Monica Smith A and Gerald E. Edwards A DA School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236, USA.
B Present address: Department of Biology, University of Waterloo, 200 University Avenue West, Waterloo, Ontario N2L 3G1, Canada.
C Department of Biology, Faculty of Science, University of Tehran, P.O. Box 14155-6455, Tehran, Iran.
D Corresponding author. Email: edwardsg@wsu.edu
E This paper originates from an International Symposium in Memory of Vincent R. Franceschi, Washington State University, Pullman, Washington, USA, June 2006.
Functional Plant Biology 34(4) 268-281 https://doi.org/10.1071/FP06283
Submitted: 3 November 2006 Accepted: 12 January 2007 Published: 19 April 2007
Abstract
Leaves and cotyledons of the terrestrial C4 plants, Bienertia cycloptera Bunge ex Boiss. and Suaeda aralocaspica (Bunge) Freitag & Schütze (Chenopodiaceae), accomplish C4 photosynthesis within individual chlorenchyma cells: each species having a unique means of intracellular spatial partitioning of biochemistry and organelles. In this study the chlorenchyma tissue in flowers and stems of these species was investigated. Flowers have an outer whorl of green tepals with a layer of chlorenchyma cells, which are located on the abaxial side, exposed to the atmosphere. Anatomical, immunocytochemical, western blots and starch analyses show that the chlorenchyma cells in tepals are specialised for performance of single-cell C4 photosynthesis like that in leaves. In the tepals of B. cycloptera, chlorenchyma cells have a distinctive central cytoplasmic compartment, with chloroplasts which contain Rubisco, separated by cytoplasmic channels from a peripheral chloroplast-containing compartment, with phosphoenolpyruvate carboxylase (PEPC) distributed throughout the cytoplasm. In the tepals of S. aralocaspica, chlorenchyma cells have chloroplasts polarised towards opposite ends of the cells. Rubisco is found in chloroplasts towards the proximal end of the cell and PEPC is found throughout the cytoplasm. Also, green stems of B. cycloptera have a single layer of the specialised C4 type chlorenchyma cells beneath the epidermis, and in stems of S. aralocaspica, chlorenchyma cells are scattered throughout the cortical tissue with chloroplasts around their periphery, typical of C3 type chlorenchyma. During reproductive development, green flowers become very conspicuous, and their photosynthesis is suggested to be important in completion of the life cycle of these single-cell C4 functioning species.
Additional keywords: anatomy, C4 plants, immunolocalisation.
Acknowledgements
This paper is dedicated to our late friend and colleague, Dr Vincent R. Franceschi. Support was received from NSF Grant IBN-0131098, NSF Grant IBN-0236959 and by the University of Tehran (Project 6104037/1/01 to HA). We also thank the Vincent R Franceschi Microscopy and Imaging Center, Washington State University, for use of facilities and for staff assistance, and additional help from Dr E Voznesenskaya and N Koteyeva.
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