Rowan F. Sage

C₄ photosynthesis is a complex specialization that enhances carbon gain in hot, often arid habitats where photorespiration rates can be high. Certain features unique to C₄ photosynthesis may reduce the potential for phenotypic plasticity and photosynthetic acclimation to environmental change relative to what is possible with C₃ photosynthesis. During acclimation, the structural and physiological integrity of the mesophyll–bundle sheath (M-BS) complex has to be maintained if C₄ photosynthesis is to function efficiently in the new environment. Disruption of the M-BS structure could interfere with metabolic co-ordination between the C₃ and C₄ cycles, decrease metabolite flow rate between the tissues, increase CO₂ leakage from the bundle sheath, and slow enzyme activity. C₄ plants have substantial acclimation potential, but in most cases lag behind the acclimation responses in C₃ plants. For example, some C₄ species are unable to maintain high quantum yields when grown in low-light conditions. Others fail to reduce carboxylase content in shade, leaving substantial over-capacity of Rubisco and PEP carboxylase in place. Shade-tolerant C₄ grasses lack the capacity for maintaining a high state of photosynthetic induction following sunflecks, and thus may be poorly suited to exploit subsequent sunflecks compared with C₃ species. In total, the evidence indicates that C₄ photosynthesis is less phenotypically plastic than C₃ photosynthesis, and this may contribute to the more restricted ecological and geographical distribution of C₄ plants across the Earth.

The temperature response of net CO₂ assimilation rate (A), the rate of whole-chain electron transport, the activity and activation state of Rubisco, and the pool sizes of ribulose-1,5-bisphosphate (RuBP) and 3-phosphoglyceric acid (PGA) were assessed in sweet potato (Ipomoea batatas) grown under greenhouse conditions. Above the thermal optimum of photosynthesis, the activation state of Rubisco declined with increasing temperature. Doubling CO₂ above 370 μbar further reduced the activation state, while reducing CO₂ by one-half increased it. At cool temperature (2 levels where photosynthesis was unaffected by a 90% reduction in O₂ content. Reduction of the partial pressure of CO₂ at cool temperature also enhanced the activation state of Rubisco. The rate of electron transport showed a pronounced temperature response with the same temperature optimum as A at elevated CO₂. RuBP pool size and the RuBP-to-PGA ratio declined with increasing temperature. Increasing CO₂ also reduced the RuBP pool size. These results are consistent with the hypothesis that the reduction in the activation state of Rubisco at high and low temperature is a regulated response to a limitation in one of the processes contributing to the rate of RuBP regeneration. To further evaluate this possibility, we used measured estimates of Rubisco capacity, electron transport capacity, and the inorganic phosphate regeneration capacity to model the response of A to temperature. At elevated CO₂, the activation state of Rubisco declined at high temperatures where electron transport capacity was predicted to be limiting, and at cooler temperatures where the inorganic phosphate regeneration capacity was limiting. At low CO₂, where Rubisco capacity was predicted to limit photosynthesis, full activation of Rubisco was observed at all measurement temperatures.

Xylem structure and function is proposed to reflect an evolutionary balance between demands for efficient movement of water to the leaf canopy and resistance to cavitation during high xylem tension. Water use efficiency (WUE) affects this balance by altering the water cost of photosynthesis. Therefore species of greater WUE, such as C₄ plants, should have altered xylem properties. To evaluate this hypothesis, we assessed the hydraulic and anatomical properties of 19 C₃ and C₄ woody species from arid regions of the American west and central Asia. Specific conductivity of stem xylem (K _s ) was 16%–98% lower in the C₄ than C₃ shrubs from the American west. In the Asian species, the C₃ Nitraria schoberi had similar and Halimodendron halodendron higher K _s values compared with three C₄ species. Leaf specific conductivity (K _L ; hydraulic conductivity per leaf area) was 60%–98% lower in the C₄ than C₃ species, demonstrating that the presence of the C₄ pathway alters the relationship between leaf area and the ability of the xylem to transport water. C₄ species produced similar or smaller vessels than the C₃ shrubs except in Calligonum, and most C₄ shrubs exhibited higher wood densities than the C₃ species. Together, smaller conduit size and higher wood density indicate that in most cases, the C₄ shrubs exploited higher WUE by altering xylem structure to enhance safety from cavitation. In a minority of cases, the C₄ shrubs maintained similar xylem properties but enhanced the canopy area per branch. By establishing a link between C₄ photosynthesis and xylem structure, this study indicates that other phenomena that affect WUE, such as atmospheric CO₂ variation, may also affect the evolution of wood structure and function.

Plants using the C₄ photosynthetic pathway have greater water use efficiency (WUE) than C₃ plants of similar ecological function. Consequently, for equivalent rates of photosynthesis in identical climates, C₄ plants do not need to acquire and transport as much water as C₃ species. Because the structure of xylem tissue reflects hydraulic demand by the leaf canopy, a reduction in water transport requirements due to C₄ photosynthesis should affect the evolution of xylem characteristics in C₄ plants. In a comparison of stem hydraulic conductivity and vascular anatomy between eight C₃ and eight C₄ herbaceous species, C₄ plants had lower hydraulic conductivity per unit leaf area (K_L) than C₃ species of similar life form. When averages from all the species were pooled together, the mean K_L for the C₄ species was 1.60 × 10⁻⁴ kg m⁻¹ s⁻¹ MPa⁻¹, which was only one‐third of the mean K_L of 4.65 × 10⁻⁴ kg m⁻¹ s⁻¹ MPa⁻¹ determined for the C₃ species. The differences in K_L between C₃ and C₄ species corresponded to the two‐ to three‐fold differences in WUE observed between C₃ and C₄ plants. In the C₄ species from arid regions, the difference in K_L was associated with a lower hydraulic conductivity per xylem area, smaller and shorter vessels, and less vulnerable xylem to cavitation, indicating the C₄ species had evolved safer xylem than the C₃ species. In the plants from resource‐rich areas, such as the C₄ weed Amaranthus retroflexus, hydraulic conductivity per xylem area and xylem anatomy were similar to that of the C₃ species, but the C₄ plants had greater leaf area per xylem area. The results indicate the WUE advantage of C₄ photosynthesis allows for greater flexibility in hydraulic design and potential fitness. In resource‐rich environments in which competition is high, an existing hydraulic design can support greater leaf area, allowing for higher carbon gain, growth and competitive potential. In arid regions, C₄ plants evolved safer xylem, which can increase survival and performance during drought events.

C4 plants are directly affected by all major global change parameters, often in a manner that is distinct from that of C3 plants. Rising CO2 generally stimulates C3 photosynthesis more than C4, but C4...

C₄ plants are uncommon in cold environments and do not generally occur in the alpine tundra. In the White Mountains of California, however, the C₄ grass Muhlenbergia richardsonis is common in the alpine zone at 3,300–3,800 m, with the highest population observed at 3,960 m (13,000 feet) above sea level. This is the highest reported C₄ species in North America and is near the world altitude limit for C₄ plants (4,000–4,500 m). Above 3,800 m, M. richardsonis is largely restricted to southern slope aspects, with greatest frequency on southeast-facing slopes. In open tundra, M. richardsonis formed prostrate mats with a mean height of 2.5 cm. Neighboring C₃ grasses were two to three times taller. Because of its short stature, leaf temperature of M. richardsonis was greatly influenced by the boundary layer of the ground, rising over 20°C above air temperature in full sun and still air and over 10°C above air temperature in full sun and wind velocity of 1–4 m s^–1. Thus, although air temperatures did not exceed 15°C, midday leaf temperatures of M. richardsonis were routinely between 25°C and 35°C, a range favorable to C₄ photosynthesis. At night, leaf temperature of M. richardsonis was often 5–12°C below air temperature, resulting in regular exposure to subzero temperatures and frosting of the leaves. No visible injury was associated with exposure to freezing night temperatures. The presence of M. richardsonis in the alpine zone demonstrates that C₄ plants can tolerate extreme cold during the growing season. The localization to microsites where leaf temperatures can exceed 25°C during the day, however, indicates that even when cold tolerant, C₄ plants still require periods of high leaf temperature to remain competitive with C₃ species. In this regard, the prostrate growth form of M. richardsonis compensates for the alpine climate by allowing sufficient heating of the leaf canopy during the day.

Atmospheric [CO₂] affects photosynthesis and therefore should affect the supply of carbon to roots. To evaluate interactions between carbon supply and nutrient acquisition, the [CO₂] effects on root growth, proteoid root formation and phosphorus (P) uptake capacity were studied in white lupin (Lupinus albus L.) grown hydroponically at 200, 410 and 750 µmol mol⁻¹ CO₂, under sufficient (0·25 mm P) and deficient (0·69 µm P) phosphorus. Plant size increased with increasing [CO₂] only at high P. Both P deficiency and increasing [CO₂] increased the production of proteoid clusters; the increase in response to increased [CO₂] was proportionally greater from low to ambient [CO₂] than from ambient to high. The activity of phosphoenol pyruvate carboxylase in the proteoid root, the exudation of organic acids from the roots, and the specific uptake of P increased with P deficiency, but were unaffected by [CO₂]. Increasing [CO₂] from Pleistocene levels to those predicted for the next century increased plant size and allocation to proteoid roots, but did not change the specific P uptake capacity per unit root mass. Hence, rising [CO₂] should promote nutrient uptake by allowing lupins to mine greater volumes of soil.