Contents

Summary 341

I.  Introduction 342
II.  What is C4 photosynthesis? 343
III.  Why did C4 photosynthesis evolve? 347
IV.  Evolutionary lineages of C4 photosynthesis 348
V.  Where did C4 photosynthesis evolve? 350
VI.  How did C4 photosynthesis evolve? 352
VII.  Molecular evolution of C4 photosynthesis 361
VIII. When did C4 photosynthesis evolve 362
IX.  The rise of C4 photosynthesis in relation to climate and CO2 363
X.  Final thoughts: the future evolution of C4 photosynthesis 365

Acknowledgements 365


References 365



Summary
C4 photosynthesis is a series of anatomical and biochemical modifications that concentrate CO2 around the carboxylating enzyme Rubisco, thereby increasing photosynthetic efficiency in conditions promoting high rates of photorespiration. The C4 pathway independently evolved over 45 times in 19 families of angiosperms, and thus represents one of the most convergent of evolutionary phenomena. Most origins of C4 photosynthesis occurred in the dicots, with at least 30 lineages. C4 photosynthesis first arose in grasses, probably during the Oligocene epoch (24–35 million yr ago). The earliest C4 dicots are likely members of the Chenopodiaceae dating back 15–21 million yr; however, most C4 dicot lineages are estimated to have appeared relatively recently, perhaps less than 5 million yr ago. C4 photosynthesis in the dicots originated in arid regions of low latitude, implicating combined effects of heat, drought and/or salinity as important conditions promoting C4 evolution. Low atmospheric CO2 is a significant contributing factor, because it is required for high rates of photorespiration. Consistently, the appearance of C4 plants in the evolutionary record coincides with periods of increasing global aridification and declining atmospheric CO2. Gene duplication followed by neo- and nonfunctionalization are the leading mechanisms for creating C4 genomes, with selection for carbon conservation traits under conditions promoting high photorespiration being the ultimate factor behind the origin of C4 photosynthesis.

The evolution of C4 photosynthesis

https://febs.onlinelibrary.wiley.com/doi/pdf/10.1016/S0014-5793%2800%2902331-0

NADP-malic enzyme from plants: a ubiquitous enzyme involved in different metabolic pathways.

What can enzymes of C4 photosynthesis do for C3 plants under stress

The Arabidopsis (Arabidopsis thaliana) genome contains four genes encoding putative NADP-malic enzymes (MEs; AtNADP-ME1–ME4). NADP-ME4 is localized to plastids, whereas the other three isoforms do not possess any predicted organellar targeting sequence and are therefore expected to be cytosolic. The plant NADP-MEs can be classified into four groups: groups I and II comprising cytosolic and plastidic isoforms from dicots, respectively; group III containing isoforms from monocots; and group IV composed of both monocots and dicots, including AtNADP-ME1. AtNADP-MEs contained all conserved motifs common to plant NADP-MEs and the recombinant isozymes showed different kinetic and structural properties. NADP-ME2 exhibits the highest specific activity, while NADP-ME3 and NADP-ME4 present the highest catalytic efficiency for NADP and malate, respectively. NADP-ME4 exists in equilibrium of active dimers and tetramers, while the cytosolic counterparts are present as hexamers or octamers. Characterization of T-DNA insertion mutant and promoter activity studies indicates that NADP-ME2 is responsible for the major part of NADP-ME activity in mature tissues of Arabidopsis. Whereas NADP-ME2 and -ME4 are constitutively expressed, the expression of NADP-ME1 and NADP-ME3 is restricted by both developmental and cell-specific signals. These isoforms may play specific roles at particular developmental stages of the plant rather than being involved in primary metabolism.

A Comprehensive Analysis of the NADP-Malic Enzyme Gene Family of Arabidopsis

Our most productive crops and native vegetation use a modified version of photosynthesis known as the C4 pathway. Leaves of C4 crops have increased nitrogen and water use efficiencies compared with C3 species. Although the modifications to leaves of C4 plants are complex, their faster growth led to the proposal that C4 photosynthesis should be installed in C3 crops in order to increase yield potential. Typically, a limited set of proteins become restricted to mesophyll or bundle sheath cells, and this allows CO2 to be concentrated around the primary carboxylase RuBisCO. The role that these proteins play in C3 species prior to their recruitment into the C4 pathway is addressed here. Understanding the role of these proteins in C3 plants is likely to be of use in predicting how the metabolism of a C3 leaf will alter as components of the C4 pathway are introduced as part of efforts to install characteristics of C4 photosynthesis in leaves of C3 crops.

The role of proteins in C3 plants prior to their recruitment into the C4 pathway

NADP-malic enzyme from plants.

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NADP-malic enzyme from plants.