The evolution of C 4 photosynthesis in many taxa involves the establishment of a two-celled photorespiratory CO 2 pump, termed C 2 photosynthesis. How C 3 species evolved C 2 metabolism is critical to understanding the initial phases of C 4 plant evolution. To evaluate early events in C 4 evolution, we compared leaf anatomy, ultrastructure, and gas-exchange responses of closely related C 3 and C 2 species of Flaveria, a model genus for C 4 evolution. We hypothesized that Flaveria pringlei and Flaveria robusta, two C 3 species that are most closely related to the C 2 Flaveria species, would show rudimentary characteristics of C 2 physiology. Compared with less-related C 3 species, bundle sheath (BS) cells of F. pringlei and F. robusta had more mitochondria and chloroplasts, larger mitochondria, and proportionally more of these organelles located along the inner cell periphery. These patterns were similar, although generally less in magnitude, than those observed in the C 2 species Flaveria angustifolia and Flaveria sonorensis. In F. pringlei and F. robusta, the CO 2 compensation point of photosynthesis was slightly lower than in the less-related C 3 species, indicating an increase in photosynthetic efficiency. This could occur because of enhanced refixation of photorespired CO 2 by the centripetally positioned organelles in the BS cells. If the phylogenetic positions of F. pringlei and F. robusta reflect ancestral states, these results support a hypothesis that increased numbers of centripetally located organelles initiated a metabolic scavenging of photorespired CO 2 within the BS. This could have facilitated the formation of a glycine shuttle between mesophyll and BS cells that characterizes C 2 photosynthesis.
SummaryTriploid Miscanthus hybrids have superior chilling tolerance across Miscanthus and Saccharum genotypes bred for cool temperate climates.
There is much interest in cultivating C4 perennial plants in northern climates where there is an abundance of land and a potential large market for biofuels. C4 feedstocks can exhibit superior yields to C3 alternatives during the long warm days of summer at high latitude, but their summer success depends on an ability to tolerate deep winter cold, spring frosts, and early growth-season chill. Here, we review cold tolerance limits in C4 perennial grasses. Dozens of C4 species are known from high latitudes to 63 °N and elevations up to 5200 m, demonstrating that C4 plants can adapt to cold climates. Of the three leading C4 grasses being considered for bioenergy production in cold climates--Miscanthus spp., switchgrass (Panicum virgatum), and prairie cordgrass (Spartina pectinata)--all are tolerant of cool temperatures (10-15 °C), but only cordgrass tolerates hard spring frosts. All three species overwinter as dormant rhizomes. In the productive Miscanthus×giganteus hybrids, exposure to temperatures below -3 °C to -7 °C will kill overwintering rhizomes, while for upland switchgrass and cordgrass, rhizomes survive exposure to temperatures above -20 °C to -24 °C. Cordgrass emerges earlier than switchgrass and M. giganteus genotypes, but lacks the Miscanthus growth potential once warmer days of late spring arrive. To enable C4-based bioenergy production in colder climates, breeding priorities should emphasize improved cold tolerance of M.×giganteus, and enhanced productivity of switchgrass and cordgrass. This should be feasible in the near future, because wild populations of each species exhibit a diverse range of cold tolerance and growth capabilities.
Highlight Spartina pectinata (prairie cordgrass) has superior rhizome freezing tolerance, spring leaf frost and freezing tolerance, and greater first year establishment compared to Miscanthus × giganteus at a cool temperate site.
Miscanthus is a C4 perennial grass being developed for bioenergy production in temperate regions where chilling events are common. To evaluate chilling effects on Miscanthus, we assessed the processes controlling net CO2 assimilation rate (A) in Miscanthus x giganteus (M161) and a chilling-sensitive Miscanthus hybrid (M115) before and after a chilling treatment of 12/5 °C. The temperature response of A and maximum Rubisco activity in vitro were identical below 20 °C in chilled and unchilled M161, demonstrating Rubisco capacity limits or co-limits A at cooler temperatures. By contrast, A in M115 decreased at all measurement temperatures after growth at 12/5 °C. Rubisco activity in vitro declined in proportion to the reduction in A in chilled M115 plants, indicating Rubisco capacity is responsible in part for the decline in A. Pyruvate orthophosphate dikinase activities were also reduced by the chilling treatment when assayed at 28 °C, indicating this enzyme may also contribute to the reduction in A in M115. The maximum extractable activities of PEPCase and NADP-ME remained largely unchanged after chilling. The carboxylation efficiency of the C4 cycle was depressed in both genotypes to a similar extent after chilling. ΦP :ΦCO2 remained unchanged in both genotypes indicating the C3 and C4 cycles decline equivalently upon chilling.
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