Despite phylogenetic effects, C3-C4 lineages bridge the ecological gap to C4 photosynthesis.

Marjorie R Lundgren,Pascal-Antoine Christin

doi:10.1093/jxb/erw451

Abstract

C4 photosynthesis is a physiological innovation involving several anatomical and biochemical components that emerged recurrently in flowering plants. This complex trait evolved via a series of physiological intermediates, broadly termed 'C3-C4', which have been widely studied to understand C4 origins. While this research program has focused on biochemistry, physiology, and anatomy, the ecology of these intermediates remains largely unexplored. Here, we use global occurrence data and local habitat descriptions to characterize the niches of multiple C3-C4 lineages, as well as their close C3 and C4 relatives. While C3-C4 taxa tend to occur in warm climates, their abiotic niches are spread along other dimensions, making it impossible to define a universal C3-C4 niche. Phylogeny-based comparisons suggest that, despite shifts associated with photosynthetic types, the precipitation component of the C3-C4 niche is particularly lineage specific, being highly correlated with that of closely related C3 and C4 taxa. Our large-scale analyses suggest that C3-C4 lineages converged toward warm habitats, which may have facilitated the transition to C4 photosynthesis, effectively bridging the ecological gap between C3 and C4 plants. The intermediates retained some precipitation aspects of their C3 ancestors' habitat, and likely transmitted them to their C4 descendants, contributing to the diversity among C4 lineages seen today.

Highlights

The C4 photosynthetic pathway relies on a coordinated system of anatomical and biochemical traits that function to concentrate CO2 around Rubisco, which in most C4 plants is localized to the bundle sheath cells (Hatch, 1987)
C3–C4 intermediates occur at high elevations, along the Andes mountains (e.g. Steinchisma decipiens, Steinchisma hians, Mollugo verticillata, Diplotaxis muralis), in Lesotho (e.g. Diplotaxis muralis, Blepharis espinosa), and in the highlands of Mexico (e.g. Mollugo verticillata, Berkheya spinosissma; Table 2; Supplementary Figs S1 and S2; Supplementary Dataset S1)
We present the first systematic description of the geographical and ecological distribution of C3–C4 intermediates

Summary

Introduction

The C4 photosynthetic pathway relies on a coordinated system of anatomical and biochemical traits that function to concentrate CO2 around Rubisco, which in most C4 plants is localized to the bundle sheath cells (Hatch, 1987). CO2 concentration substantially suppresses O2 fixation and subsequent photorespiration, compared with the ancestral C3 photosynthetic pathway, making C4 photosynthesis advantageous in conditions that increase photorespiration (Chollet and Ogren, 1975; Hatch and Osmond, 1976). It has been widely reported that some plants possess only a subset of the anatomical and/or biochemical components of the C4 pump. These plants tend to be physiologically somewhere in between typical C3 and C4 plants and, as such, are termed C3–C4 intermediates (Kennedy and Laetsch, 1974; Monson and Moore, 1989; Sage, 2004; Schlüter and Weber, 2016)

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