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

C(4) photosynthesis is one of the most convergent evolutionary phenomena in the biological world, with at least 66 independent origins. Evidence from these lineages consistently indicates that the C(4) pathway is the end result of a series of evolutionary modifications to recover photorespired CO(2) in environments where RuBisCO oxygenation is high. Phylogenetically informed research indicates that the repositioning of mitochondria in the bundle sheath is one of the earliest steps in C(4) evolution, as it may establish a single-celled mechanism to scavenge photorespired CO(2) produced in the bundle sheath cells. Elaboration of this mechanism leads to the two-celled photorespiratory concentration mechanism known as C(2) photosynthesis (commonly observed in C(3)-C(4) intermediate species) and then to C(4) photosynthesis following the upregulation of a C(4) metabolic cycle.

Photorespiration and the Evolution of C4 Photosynthesis

Plants assimilate carbon by one of three photosynthetic pathways, commonly called the C 3 , C 4 , and CAM pathways The C 4 photosynthetic pathway, found only among the angiosperms, represents a modification of C 3 metabolism that is most effective at low concentrations of CO 2  Today, C 4 plants are most common in hot, open ecosystems, and it is commonly felt that they evolved under these conditions However, high light and high temperature, by themselves, are not sufficient to favor the evolution of C 4 photosynthesis at atmospheric CO 2 levels significantly above the current ambient values A review of evidence suggests that C 4 plants evolved in response to a reduction in atmospheric CO 2 levels that began during the Cretaceous and continued until the Miocene

Climate change and the evolution of C4 photosynthesis

Using isotopic screens, phylogenetic assessments, and 45 years of physiological data, it is now possible to identify most of the evolutionary lineages expressing the C 4 photosynthetic pathway. Here, 62 recognizable lineages of C 4 photosynthesis are listed. Thirty-six lineages (60%) occur in the eudicots. Monocots account for 26 lineages, with a minimum of 18 lineages being present in the grass family and six in the sedge family. Species exhibiting the C 3 ‐C 4 intermediate type of photosynthesis correspond to 21 lineages. Of these, 9 are not immediately associated with any C 4 lineage, indicating that they did not share common C 3 ‐C 4 ancestors with C 4 species and are instead an independent line. The geographic centre of origin for 47 of the lineages could be estimated. These centres tend to cluster in areas corresponding to what are now arid to semi-arid regions of southwestern North America, southcentral South America, central Asia, northeastern and southern Africa, and inland Australia. With 62 independent lineages, C 4 photosynthesis has to be considered one of the most convergent of the complex evolutionary phenomena on planet Earth, and is thus an outstanding system to study the mechanisms of evolutionary adaptation.

/pdf/the-c4-plant-lineages-of-planet-earth-4eeeble5zv.pdf

The C4 plant lineages of planet Earth

Phylogenetic and Systematic Inferences from Electrophoretic Studies

Systematics of Flaveria (Flaveriinae-Asteraceae)

Reports of 150 original chromosome counts are recorded, including reports of 22 genera and 57 species and subspecific taxa in tribe Lactuceae. Also included are first reports for 12 specific or subspecific taxa. x = 9 appears to be the ancestral base of the tribe. Chromosome numbers are known for over 85% of the genera of the tribe and the frequency of polyploidy is ca. 23%, which is about one-half that of the angiosperms.

Chromosome numbers in the compositae.

Chromosome Numbers in Compositae. XIII. Eupatorieae

Chromosome numbers are reported for 112 collections of Cactaceae, including 102 collections of Opuntia. Reports are presented for 33 species in five genera and a total of 36 taxa. Two specimens were sterile. Emphasis was given to the documentation of intraspecific ploidy-level consistencies and differences, because of the current poor state of knowledge about the populational integrity of chromosome numbers in Trans-Pecos cacti and because information about ploidy levels is taxonomically significant particularly in certain genera of Cactaceae. First reports are presented for six taxa, including Opuntia aureispina (2n = 11 II), O. tortispina (2n = 33 II), and Ancistrocactus tobuschii (2n = 11 II). Chromosome numbers are now known for all but one or two of the ∼104 currently recognized cactus taxa in Trans-Pecos Texas.

https://bsapubs.onlinelibrary.wiley.com/doi/pdf/10.2307/2657113

A. Michael Powell

Papers

Systematics of Flaveria (Flaveriinae-Asteraceae)

Chromosome numbers in the compositae.

Chromosome Numbers in Compositae. XIII. Eupatorieae

Chromosome numbers in Chihuahuan Desert Cactaceae. III. Trans-Pecos Texas.

6-methoxyflavonoids from Brickellia laciniata (Compositae)