Development of structural and biochemical characteristics of C4 photosynthesis in two types of Kranz anatomy in genus Suaeda (family Chenopodiaceae)

Abstract

Genus Suaeda (family Chenopodiaceae, subfamily Suaedoideae) has two structural types of Kranz anatomy consisting of a single compound Kranz unit enclosing vascular tissue. One, represented by Suaeda taxifolia, has mesophyll (M) and bundle sheath (BS) cells distributed around the leaf periphery. The second, represented by Suaeda eltonica, has M and BS surrounding vascular bundles in the central plane. In both, structural and biochemical development of C(4) occurs basipetally, as observed by analysis of the maturation gradient on longitudinal leaf sections. This progression in development was also observed in mid-sections of young, intermediate, and mature leaves in both species, with three clear stages: (i) monomorphic chloroplasts in the two cell types in younger tissue with immunolocalization and in situ hybridization showing ribulose bisphosphate carboxylase oxygenase (Rubisco) preferentially localized in BS chloroplasts, and increasing in parallel with the establishment of Kranz anatomy; (ii) vacuolization and selective organelle positioning in BS cells, with occurrence of phosphoenolpyruvate carboxylase (PEPC) and immunolocalization showing that it is preferentially in M cells; (iii) establishment of chloroplast dimorphism and mitochondrial differentiation in mature tissue and full expression of C(4) biochemistry including pyruvate, Pi dikinase (PPDK) and NAD-malic enzyme (NAD-ME). Accumulation of rbcL mRNA preceded its peptide expression, occurring prior to organelle positioning and differentiation. During development there was sequential expression and increase in levels of Rubisco and PEPC followed by NAD-ME and PPDK, and an increase in the (13)C/(12)C isotope composition of leaves to values characteristic of C(4) photosynthesis. The findings indicate that these two forms of NAD-ME type C(4) photosynthesis evolved in parallel within the subfamily with similar ontogenetic programmes.

Differentiation of C4 photosynthesis along a leaf developmental gradient in two Cleome species having different forms of Kranz anatomy

“…Sample preparation for light microscopy (LM) and transmission electron microscopy (TEM) was carried out following Koteyeva et al (2011 a ). An Olympus BH-2 (Olympus Optical Co. Ltd) light microscope equipped with an LM Digital Camera and Software (Jenoptik ProgRes Camera, C12plus, Jena, Germany) was used for observation and collection of images at the LM level.…”

“…Sample preparation and immunolocalization by LM and TEM were carried out on longitudinal sections of leaves, 6–7mm long, following the procedure in Koteyeva et al (2011 a ). Antibodies used were anti-spinach Rubisco [large subunit (LSU)] IgG (courtesy of B. McFadden) commercially available anti-maize PEPC IgG (Chemicon, Temecula, CA, USA), and the P-subunit of GDC, all raised in rabbits.…”

“…There has been less attention to development of types of Kranz anatomy which surround all veins in the leaves. There are reports on NADP-ME Salsoloid type with Salsola richteri (Voznesenskaya et al , 2003b), NAD-ME Salsinoid type with Suaeda taxifolia , and NAD-ME Schoberioid type with Suaeda eltonica (Koteyeva et al , 2011 a ). …”

“…Characterization of the development of Kranz anatomy includes identification of the origins of M and BS cells during leaf initiation, which is different depending on Kranz anatomical type or plant lineages (Dengler et al , 1985; Dengler and Nelson, 1999; Soros and Dengler, 2001; Koteyeva et al , 2011 a ). This characterization includes structural differentiation of M and BS chloroplasts and their function in photochemistry to provide energy cooperatively for CO 2 assimilation (Brown, 1975; Dengler et al , 1985; Langdale et al , 1988 a , b ; Dengler and Nelson, 1999; Sheen, 1999; von Caemmerer and Furbank, 2003; Patel and Berry, 2008; Li et al , 2010; Majeran et al , 2010; Edwards and Voznesenskaya, 2011; Koteyeva et al , 2011 a ; Wang et al , 2013). It also consists of analysis of the differences among forms of C 4 in the development of barriers to diffusion of CO 2 from sites of decarboxylation in BS cells, which enables CO 2 to be concentrated around Rubisco (e.g.…”

“…BS cell wall thickness, location of the C 4 acid decarboxylase, and the position of organelles) (von Caemmerer and Furbank, 2003). Determining when selective expression of enzymes in M and BS cells for C 4 function occurs during development among different forms of C 4 is also important (Dengler et al , 1985; Soros and Dengler, 2001; Koteyeva et al , 2011 a ; Langdale, 2012). Analyses show that there are differences in the sequence and the timing of biochemical and structural changes, with respect to establishment of the vascular system, and whether expression of traits is regulated by environmental (light) or developmental cues (Langdale et al , 1988 a ; Wang et al , 1992; Dengler et al , 1995; Ramsperger et al , 1996; Dengler and Nelson, 1999; Sheen, 1999; Voznesenskaya et al , 2003 a ; Wakayama et al , 2003; Koteyeva et al , 2011 a ; Langdale, 2012).…”