C₄ Cycles: Past, Present, and Future Research on C₄ Photosynthesis

Abstract

In the late 1960s, a vibrant new research field was ignited by the discovery that instead of fixing CO 2 into a C 3 compound, some plants initially fix CO 2 into a four-carbon (C 4 ) compound. The term C 4 photosynthesis was born. In the 20 years that followed, physiologists, biochemists, and molecular and developmental biologists grappled to understand how the C 4 photosynthetic pathway was partitioned between two morphologically distinct cell types in the leaf. By the early 1990s, much was known about C 4 biochemistry, the types of leaf anatomy that facilitated the pathway, and the patterns of gene expression that underpinned the biochemistry. However, virtually nothing was known about how the pathway was regulated. It should have been an exciting time, but many of the original researchers were approaching retirement, C 4 plants were proving recalcitrant to genetic manipulation, and whole-genome sequences were not even a dream. In combination, these factors led to reduced funding and the failure to attract young people into the field; the endgame seemed to be underway. But over the last 5 years, there has been a resurgence of interest and funding, not least because of ambitious multinational projects that aim to increase crop yields by introducing C 4 traits into C 3 plants. Combined with new technologies, this renewed interest has resulted in the development of more sophisticated approaches toward understanding how the C 4 pathway evolved, how it is regulated, and how it might be manipulated. The extent of this resurgence is manifest by the publication in 2011 of more than 650 pages of reviews on different aspects of C 4 . Here, I provide an overview of our current understanding, the questions that are being addressed, and the issues that lie ahead.

Sodium as nutrient and toxicant

“…Recently, in a benchmark study, Furumoto et al (2011) characterized the Na + -pyruvate cotransport mechanism at the molecular level, by identification of the BASS2 gene in Flaveria and Cleome, and showing the protein's localization to the chloroplast envelope and the facilitation of pyruvate influx. They showed widespread distribution of the gene across various plant groups, but also its absence, at the protein expression level, in corn, in agreement with the earlier physiological observations, and in keeping with the great diversity known to exist among C 4 species (Weber and von Caemmerer 2010), and the multiple evolutionary origins of the trait (Langdale 2011;Sage et al 2011;Williams et al 2012). However, there now appears little doubt that the mechanism of Na + -dependent pyruvate transport is central to the Na + requirement in many C 4 species.…”

Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential

“…Small collections of other resources, including simple sequence repeats 10 and expressed sequence tags (ESTs) 11 , have also been developed. The process of C 4 photosynthesis and genes in C4 pathway has been investigated 12 . The availability of genome sequences has enabled the identification of gene duplication and neofunctionalization events that have contributed to the evolution of several enzymes involved in C 4 photosynthesis 13 .…”

Recruitment of pre-existing networks during the evolution of C 4 photosynthesis

“…Despite its complexity, the C 4 pathway has evolved independently in more than 60 lineages that span 18 plant families [16], making it one of the most remarkable examples of convergent evolution found in biology. It is thought that the evolution of C 4 photosynthesis relied on a series of coordinated modifications to leaf anatomy, cell biology and biochemistry [17]. However, the basic components, including enzymes of the C 4 pathway, are present in species that use the ancestral C 3 pathway [18].…”