On the Inside

Yield Effects in Two Major Crops under Conditions of Projected Climate Change

Global food demand is projected to increase up to 110% by the middle of this century, particularly due to a rise in world population. Additionally, the average concentration of atmospheric CO₂ ([CO₂]) has increased 1.75 μmol mol⁻¹ per year between 1975 and today, reaching 400 μmol mol⁻¹ in April 2015. It is projected that current [CO₂] levels will double by the end of the century. The increasing atmospheric [CO₂] is causing changes in global climate, including reduction in water availability and elevation in temperature. These factors are expected to heavily influence food production in the next years. Drought is a main environmental factor responsible for decreasing crop productivity and grain quality, especially when occurring during the grain-filling stage. However, elevated [CO₂] is predicted to mitigate some of the negative effects of drought. Sorghum (Sorghum bicolor), a staple food grain for millions of the poorest and most food-insecure people in the semiarid tropics of Africa, Asia, and Central America, is a C₄ grass that has important economical and nutritional values in many parts of the world. Although the impact of elevated [CO₂] and drought in photosynthesis and sorghum growth has been well documented, the effects of the combination of these two environmental factors on plant metabolism have yet to be determined. To address this gap in our knowledge, De Souza et al. (pp. 1755–1765) grew sorghum plants at ambient (400 μmol mol⁻¹) or elevated (800 μmol mol⁻¹) [CO₂] for 120 d and then subjected them to drought during the grain-filling stage. Leaf photosynthesis, respiration, and stomatal conductance were measured at 90 and 120 d after planting, and plant organs (leaves, culm, roots, prop roots, and grains) were harvested. Biomass and intracellular metabolites were assessed for each organ. As expected, elevated [CO₂] reduced the stomatal conductance, which preserved soil moisture and plant fitness under drought. Surprisingly, whole-plant metabolism was adjusted, and protein content in grains was improved by 60% in sorghum grown under elevated [CO₂].

A second paper in this issue considers the large differences in response of soybean (Glycine max) cultivars to projected changes in [CO₂]. The purpose of this study by Kumagai et al. (pp. 2021–2029) was to identify traits responsible for elevated CO₂ responsiveness in soybean. The authors grew 12 Japanese and U.S. soybean cultivars that differed in time to maturity and determinacy under ambient CO₂ and elevated CO₂ for 2 years in temperature gradient chambers. The authors report that CO₂ elevation significantly increased seed yield per plant, and the magnitude varied widely among the cultivars (from 0%–62%). Late-maturing rice (Oryza sativa) cultivars benefited more from elevated CO₂ than early maturing cultivars because of the longer periods during which they can grow. Moreover, indeterminate soybean cultivars, because they have more sinks, exhibited superior responsiveness to elevated CO₂ than determinate cultivars. The yield increase under artificially elevated [CO₂] conditions was best explained by increased aboveground biomass and pod number per plant. These results suggest that the plasticity of pod production under elevated CO₂ results from biomass enhancement and, therefore, would be a key factor in the yield response to elevated CO₂. Unfortunately, screening plants for breeding purposes under the high [CO₂] levels attainable in growth chambers is not practicable, but the authors describe an interesting trick to bypass this problem. Individual plant growth is usually restricted by interplant competition for solar radiation, soil nutrients, and water, so a lower planting density could potentially increase the source strength for individual plants by increasing the availability of resources. Thus, lower plant density can imitate the greater resource availability that would occur under elevated CO₂. To test this hypothesis, the authors grew the same cultivars at low planting density. Low planting density significantly increased seed yield per plant, and the magnitude ranged from 5% to 105% among the cultivars because of increased biomass and pod number per plant. The yield increase due to low-density planting was significantly positively correlated with the elevated CO₂ response. These results suggest that high plasticity of biomass and pod production at a low planting density reveals suitable parameters for breeding to maximize soybean yield under elevated CO₂.

Flavonoids Extend the Shelf Life of Tomato

Among the biggest challenges faced by the tomato (Solanum lycopersicum) industry is postharvest deterioration, which accounts for massive economic losses averaging over 25% of fresh produce every year. Two processes largely determine the shelf life of tomato fruit: the rate of fruit softening during overripening and susceptibility to opportunistic pathogens such as gray mold (Botrytis cinerea). During the infection of tomato fruit by necrotrophic pathogens such as gray mold, a burst of reactive oxygen species (ROS) is generated by NADPH oxidases in both the host plant cells and in the fungal pathogen. The ROS burst is believed to facilitate the susceptibility of plants to B. cinerea. High ROS-scavenging ability is a common feature of different flavonoids and has been attributed to the high reactivity of their hydroxyl groups to ROS. In vitro analysis indicates that the number of hydroxyl groups of flavonoids is important in determining the antioxidant capacity of flavonoids and their effectiveness in scavenging free radicals. In this issue, Zhang et al. (pp. 1568–1583) compare the shelf life of tomato fruit that accumulate different flavonoids. They report that delayed overripening is associated with increased total antioxidant capacity caused by the accumulation of flavonoids in the fruit. Reduced susceptibility to B. cinerea, however, is conferred only by certain flavonoids. Thus, specific flavonoids have differential effects on extending the shelf life of tomato. These results have significance for breeding to improve the extended shelf life in tomato and in many other fleshy fruit.

Myosin and Pollen Tube Growth

Pollen tubes undergo rapid polarized tip growth to transport the two nonmotile sperm cells to an ovule. This rapid growth is supported by the constant delivery of secretory vesicles to the pollen tube tip, where they fuse with the plasma membrane to enlarge the cell. This vesicle delivery is thought to be driven by the rapid movement of organelles and cytosol throughout the cell, a process that is commonly referred to as cytoplasmic streaming. Drug treatments revealed that pollen tube cytoplasmic streaming and tip growth depend on actin filaments. It is generally assumed that myosin-driven movements along these actin filaments are required to sustain the high growth rates of pollen tubes. In Arabidopsis (Arabidopsis thaliana), six of 13 myosin XI genes are highly expressed in pollen. Madison et al. (pp. 1946–1960) tested the role of myosin in pollen tube elongation by examining seed set, pollen fitness, and pollen tube growth for knockout mutants of five of the six myosin XI genes expressed in the pollen of Arabidopsis. Single mutants had little or no reduction in overall fertility, whereas double mutants of highly similar pollen myosins had greater defects in pollen tube growth. In particular, myo11c1 myo11c2 pollen tubes grew more slowly than wild-type pollen tubes, which resulted in reduced fitness compared with the wild type and a drastic reduction in seed set. The movements of Golgi stacks and peroxisomes were also significantly reduced, and actin filaments were less organized in myo11c1 myo11c2 pollen tubes. Interestingly, the movement of fluorescently labeled vesicles and their accumulation at pollen tube tips were not affected in the myo11c1 myo11c2 double mutant, demonstrating functional specialization among myosin isoforms. Thus, class XI myosins are required for organelle motility, actin organization, and optimal growth of pollen tubes.

Plant Response to High Mn

Manganese (Mn) is an essential element for plant growth, but its availability differs greatly in space and time, depending largely on the nature and amount of Mn minerals present and on the soil’s pH and redox potential. Mn forms complexes with many organic and inorganic ligands. Cationic Mn²⁺ is the most common form readily absorbed by plant roots. Characteristic symptoms of Mn toxicity include chlorotic and distorted leaves with small necrotic lesions. Plant species differ in response to high available Mn, but the mechanisms of sensitivity and tolerance are poorly understood. The study by Blamey et al. (pp. 2006–2020) examines the distribution and speciation of Mn in fresh roots, stems, and leaves of four crop species, soybean, white lupin (Lupinus albus), narrow-leafed lupin (Lipinus angustifolius), and sunflower (Helianthus annuus), which differ in tolerance to high Mn. The authors found that differences in tolerance were due to variations in Mn distribution and speciation within leaves. In Mn-sensitive soybean, in situ analysis of fresh leaves showed high Mn in the veins and manganite [Mn(III)] accumulation in necrotic lesions. In the two lupin species, most Mn accumulated in vacuoles as either soluble Mn(II) malate or citrate. In sunflower, Mn was sequestered as Mn(III) at the base of nonglandular trichomes. Hence, tolerance to high Mn was ascribed to effective sinks for Mn in leaves, as Mn(II) within vacuoles or through oxidation of Mn(II) to Mn(III) in trichomes. These two mechanisms prevented Mn accumulation in the cytoplasm and apoplast, thereby ensuring tolerance to high Mn in the root environment.

Shade Avoidance Effects on Tomato Leaf Morphology

Plants can sense changes in light quality. Phytochrome proteins, which sense decreases in the ratio of red to far-red wavelengths in light, initiate the shade avoidance response upon detecting deflected light from competitors. Shade-avoiding plants typically exhibit increases in internode and petiole length, reduced leaf mass per area, alterations in stomatal patterning, and shoot/root resource reallocation as an adaptive response to overgrow competitors and better intercept light. The changes in leaf shape in response to shade are more ambiguous and can be radically different based on morphological context (such as simple versus complex leaves) and species. Using a meta-analysis of more than 18,000 previously published leaflet outlines, Chitwood et al. (pp. 2030–2047) demonstrate that shade avoidance alters leaf shape in domesticated tomato and its wild relatives. The authors report that the effects of decreased ratios of red to far-red wavelengths of light on leaf shape are strong, but only when multiple morphometric parameters are considered across leaflets, both within leaves and across the leaf series, of individual plants. Circularity (a measure of leaflet serration in tomato) and leaf complexity are the most strongly affected individual traits during the shade avoidance response. After observing that shade induces increases in shoot apical meristem size, the authors then sought to describe gene expression changes in early leaf primordia and the meristem using laser microdissection. They conclude that the shade avoidance effect in leaf primordia is not mediated through canonical pathways described in mature organs, but rather by the expression of KNOTTED1-LIKE HOMEOBOX and other indeterminacy genes, altering known developmental pathways responsible for patterning leaf shape. Finally, they demonstrate that shade-induced changes in leaf primordium gene expression do not overlap very much with those found in successively initiated leaf primordia, providing evidence against classic hypotheses that shaded leaf morphology results from the prolonged heteroblastic production of juvenile leaf types.