New Insights Into the Evolution of C4 Photosynthesis Offered by the Tarenaya Cluster of Cleomaceae.

Daniele F Parma,Marcelo G M V Vaz,Wellington R Clarindo,M Eric Schranz,Adriano Nunes-Nesi,Jéssica C Silva,Urte Schlüter,Philipp Westhoff,Wagner L Araújo,Priscilla Falquetto,Andreas P M Weber,Robin Van Velzen

doi:10.3389/fpls.2021.756505

Abstract

Cleomaceae is closely related to Brassicaceae and includes C3, C3–C4, and C4 species. Thus, this family represents an interesting system for studying the evolution of the carbon concentrating mechanism. However, inadequate genetic information on Cleomaceae limits their research applications. Here, we characterized 22 Cleomaceae accessions [3 genera (Cleoserrata, Gynandropsis, and Tarenaya) and 11 species] in terms of genome size; molecular phylogeny; as well as anatomical, biochemical, and photosynthetic traits. We clustered the species into seven groups based on genome size. Interestingly, despite clear differences in genome size (2C, ranging from 0.55 to 1.3 pg) in Tarenaya spp., this variation was not consistent with phylogenetic grouping based on the internal transcribed spacer (ITS) marker, suggesting the occurrence of multiple polyploidy events within this genus. Moreover, only G. gynandra, which possesses a large nuclear genome, exhibited the C4 metabolism. Among the C3-like species, we observed intra- and interspecific variation in nuclear genome size as well as in biochemical, physiological, and anatomical traits. Furthermore, the C3-like species had increased venation density and bundle sheath cell size, compared to C4 species, which likely predisposed the former lineages to C4 photosynthesis. Accordingly, our findings demonstrate the potential of Cleomaceae, mainly members of Tarenaya, in offering novel insights into the evolution of C4 photosynthesis.

Highlights

C4 photosynthesis is a complex trait with a high degree of natural variation
The Cleomaceae species selected for this study were sampled from 20 sites, which were found in four Brazilian biomes (Amazon, Atlantic Forest, Cerrado, and Caatinga) (Figure 1 and Supplementary Table S1)
Taking the steps essential for the development of the C3–C4 and C4 photosynthetic mechanisms into account and given that the studied Cleomaceae species occur in favorable environments (Figure 1) for the development of the C3–C4 photosynthetic mechanism, our results suggest that Tarenaya species as well as Cleoserrata may be pre-conditioned to evolve the characteristics associated with carbon concentrating mechanisms

Summary

Introduction

C4 photosynthesis is a complex trait with a high degree of natural variation. It has evolved independently over 60 times in 19 different botanical families, involving anatomical and biochemical changes relative to the ancestral C3 state (Sage, 2004; Sage et al, 2011, 2014). The transition from C3 to C4 photosynthesis did not likely proceed through a single step, but rather via a series of transitory stages (Sage, 2004; Gowik and Westhoff, 2011; Schuler et al, 2016) These include the development of larger bundle sheath cells (BSCs), increase in leaf venation density (VD), restriction of glycine decarboxylase to BSCs, establishment of a photorespiratory carbon pump, enhancement of phosphoenolpyruvate carboxylase activity, establishment of the C4 cycle, and optimization of the C4 syndrome (Sage, 2004; Gowik and Westhoff, 2011). Phylogenetic studies have shown that many C3–C4 plants are closely related to C4 plants (McKown et al, 2005; Marshall et al, 2007; Christin et al, 2011a; Kadereit and Freitag, 2011; Patchell et al, 2014)

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Results

Discussion

Conclusion