Structural and physiological analyses in Salsoleae (Chenopodiaceae) indicate multiple transitions among C3, intermediate, and C4 photosynthesis

Abstract

In subfamily Salsoloideae (family Chenopodiaceae) most species are C4 plants having terete leaves with Salsoloid Kranz anatomy characterized by a continuous dual chlorenchyma layer of Kranz cells (KCs) and mesophyll (M) cells, surrounding water storage and vascular tissue. From section Coccosalsola sensu Botschantzev, leaf structural and photosynthetic features were analysed on selected species of Salsola which are not performing C4 based on leaf carbon isotope composition. The results infer the following progression in distinct functional and structural forms from C3 to intermediate to C4 photosynthesis with increased leaf succulence without changes in vein density: From species performing C3 photosynthesis with Sympegmoid anatomy with two equivalent layers of elongated M cells, with few organelles in a discontinuous layer of bundle sheath (BS) cells (S. genistoides, S. masenderanica, S. webbii) > development of proto-Kranz BS cells having mitochondria in a centripetal position and increased chloroplast number (S. montana) > functional C3–C4 intermediates having intermediate CO2 compensation points with refixation of photorespired CO2, development of Kranz-like anatomy with reduction in the outer M cell layer to hypodermal-like cells, and increased specialization (but not size) of a Kranz-like inner layer of cells with increased cell wall thickness, organelle number, and selective expression of mitochondrial glycine decarboxylase (Kranz-like Sympegmoid, S. arbusculiformis; and Kranz-like Salsoloid, S. divaricata) > selective expression of enzymes between the two cell types for performing C4 with Salsoloid-type anatomy. Phylogenetic analysis of tribe Salsoleae shows the occurrence of C3 and intermediates in several clades, and lineages of interest for studying different forms of anatomy.

Notes on the typification and nomenclature of Salsola and Kali (Chenopodiaceae)

“…and Bassia prostrata (L.) A.J.Scott, respectively. Of the other four, which have long remained in Salsola, S. kali L. is currently placed in Kali; S. rosacea L., initially also assigned to Kali, forms a clade with Noaea (Wen & al., 2010;Voznesenskaya & al., 2013) and is being transferred accordingly in a companion paper; S. vermiculata L. has become Caroxylon vermiculatum (L.) Akhani & E.H.Roalson; and only one, S. soda L., remains in Salsola as currently defined.…”

The Evolutionary Origin of C4 Photosynthesis in the Grass Subtribe Neurachninae

“…An important early step proposed for C 2 evolution is the physiological activation of the BS of C 3 species (Gowik and Westhoff, 2011;Sage et al, 2014). Activation of the BS is facilitated by increases in the number and size of mitochondria and chloroplasts and repositioning of mitochondria plus a few chloroplasts to the centripetal pole of the BS, possibly to facilitate refixation of some photorespired CO 2 produced in the leaf (Muhaidat et al, 2011;Sage et al, 2013;Voznesenskaya et al, 2013;Khoshravesh et al, 2016). Together, organelle enrichment and repositioning have been termed the "proto-Kranz" phase of early C 4 evolution, and is recognized in close relatives of C 3 and C 2 species in the eudicot genera Flaveria, Heliotropium, and Salsola, and the monocot genus Steinchisma (Muhaidat et al, 2011;Sage et al, 2013;Khoshravesh et al, 2016;Schüssler et al, 2017).…”

Initial Events during the Evolution of C4 Photosynthesis in C3 Species of Flaveria

“…For example, in Steinchisma laxa, a C 3 relative of the C 2 species of Steinchisma (Poaceae), and in C 3 relatives of C 2 species in Heliotropium (Boraginaceae), BS mitochondria have shifted to the inner, centripetal pole of the BS cells (Brown et al, 1983;Muhaidat et al, 2011). C 3 Salsola species (Chenopodiaceae) that are closely related to C 4 clades also exhibit mitochondrial shifts to the inner BS (Voznesenskaya et al, 2013). These observations indicate that there is a distinct early phase of C 4 evolution termed "proto-Kranz," where enlarged BS cells have increased numbers of mitochondria in a centripetal position (Muhaidat et al, 2011;Sage et al, 2012).…”