Corrigendum: Proximal hyperspectral imaging detects diurnal and drought-induced changes in maize physiology.

[This corrects the article DOI: 10.3389/fpls.2021.640914.].

Soybean Yield Formation Physiology - A Foundation for Precision Breeding Based Improvement.

The continued improvement of crop yield is a fundamental driver in agriculture and is the goal of both plant breeders and researchers. Plant breeders have been remarkably successful in improving crop yield, as demonstrated by the continued release of varieties with improved yield potential. This has largely been accomplished through performance-based selection, without specific knowledge of the molecular mechanisms underpinning these improvements. Insight into molecular mechanisms has been provided by plant molecular, genetic, and biochemical research through elucidation of the function of genes and pathways that underlie many of the physiological processes that contribute to yield potential. Despite this knowledge, the impact of most genes and pathways on yield components have not been tested in key crops or in a field environment for yield assessment. This gap is difficult to bridge, but field-based physiological knowledge offers a starting point for leveraging molecular targets to successfully apply precision breeding technologies such as genome editing. A better understanding of both the molecular mechanisms underlying crop yield physiology and yield limiting processes under field conditions is essential for elucidating which combinations of favorable alleles are required for yield improvement. Consequently, one goal in plant biology should be to more fully integrate crop physiology, breeding, genetics, and molecular knowledge to identify impactful precision breeding targets for relevant yield traits. The foundation for this is an understanding of yield formation physiology. Here, using soybean as an example, we provide a top-down review of yield physiology, starting with the fact that yield is derived from a population of plants growing together in a community. We review yield and yield-related components to provide a basic overview of yield physiology, synthesizing these concepts to highlight how such knowledge can be leveraged for soybean improvement. Using genome editing as an example, we discuss why multiple disciplines must be brought together to fully realize the promise of precision breeding-based crop improvement.

Proximal Hyperspectral Imaging Detects Diurnal and Drought-Induced Changes in Maize Physiology.

Hyperspectral imaging is a promising tool for non-destructive phenotyping of plant physiological traits, which has been transferred from remote to proximal sensing applications, and from manual laboratory setups to automated plant phenotyping platforms. Due to the higher resolution in proximal sensing, illumination variation and plant geometry result in increased non-biological variation in plant spectra that may mask subtle biological differences. Here, a better understanding of spectral measurements for proximal sensing and their application to study drought, developmental and diurnal responses was acquired in a drought case study of maize grown in a greenhouse phenotyping platform with a hyperspectral imaging setup. The use of brightness classification to reduce the illumination-induced non-biological variation is demonstrated, and allowed the detection of diurnal, developmental and early drought-induced changes in maize reflectance and physiology. Diurnal changes in transpiration rate and vapor pressure deficit were significantly correlated with red and red-edge reflectance. Drought-induced changes in effective quantum yield and water potential were accurately predicted using partial least squares regression and the newly developed Water Potential Index 2, respectively. The prediction accuracy of hyperspectral indices and partial least squares regression were similar, as long as a strong relationship between the physiological trait and reflectance was present. This demonstrates that current hyperspectral processing approaches can be used in automated plant phenotyping platforms to monitor physiological traits with a high temporal resolution.

Chilling stress response of postemergent cotton seedlings.

Early season development of cotton is often impaired by sudden episodes of chilling temperature. We determined the chilling response specific to postemergent 13-day-old cotton (Gossypium hirsutum L. cv. Coker 100A-glandless) seedlings. Seedlings were gradually chilled during the dark period and rewarmed during the night-to-day transition. For some chilled plants, the soil temperature was maintained at control level. Plant growth, water relations and net photosynthesis (P(n)) were analyzed after one or three chilling cycles and after 3 days of recovery. Three chilling cycles led to lower relative growth rate (RGR) compared with controls during the recovery period, especially for plants with chilled shoots and roots. Treatment differences in RGR were associated with net assimilation rate rather than specific leaf area. Both chilling treatments led to loss of leaf turgor during the night-to-day transition; this effect was greater for plants with chilled compared with warm roots. Chilling-induced water stress was associated with accumulation of the osmolyte glycine betaine to the same extent for both chilling treatments. Inhibition of P(n) during chilling was related to both stomatal and non-stomatal effects. P(n) fully recovered after seedlings were returned to control conditions for 3 days. We conclude that leaf expansion during the night-to-day transition was a significant factor determining the magnitude of the chilling response of postemergent cotton seedlings.

The piercing-sucking herbivores Lygus hesperus and Nezara viridula induce volatile emissions in plants.

Plant volatiles induced by herbivory are often used as olfactory cues by foraging herbivores and their natural enemies, and thus have potential for control of agricultural pests. Compared to chewing insects and mites, little is known about plant volatile production following herbivory by insects with piercing-sucking mouthparts. Here, we studied factors (insect life stage, gender, the role of salivary glands, and type of bioassay used for volatile induction) that influence the induction of plant volatiles by two agriculturally important hemipterans, Lygus hesperus and Nezara viridula. Feeding on intact cotton by virgin females of L. hesperus induced 2.6-fold greater volatile response compared to that induced by mated females, possibly due to increased feeding activity by virgin females. This plant volatile response was associated with elicitors present in the insect's salivary glands as well as to the degree of mechanical injury. Feeding injury by N. viridula females also increased volatile emissions in intact maize by approximately 2-fold compared to control plants. Maize seedlings injured by N. viridula emitted higher amounts of the monoterpene linalool, the sesquiterpenes (E)-beta-caryophyllene, alpha-trans-bergamotene, and (E,E)-beta-farnesene, and the homoterpene (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene, but not amounts of green leaf volatiles, compared to uninjured plants. Emissions from intact maize injured by adult males were lower than those emitted by adult females of the same age and did not differ from those emitted by uninjured plants. Similarly, feeding by virgin female N. viridula followed by excision led to 64% higher quantities of volatiles compared to untreated plants. Volatile emission in excised plants, however, was considerably greater than in intact plants, suggesting that careful consideration must be given to bioassay design in studies of herbivore-induced plant volatiles. Salivary gland extracts of N. viridula led to sesquiterpene emissions approximately 2.5-fold higher than for controls, although no significant differences were observed for green leaf volatiles, monoterpenes, and homoterpenes. These results indicate that L. hesperus and female N. viridula feeding induce volatile production in plants, and that volatile production is affected by gender and life stage of the bug. Although oviposition and mechanical injury by stylets may increase release of volatiles, elicitors from salivary glands of L. hesperus and N. viridula also seem to play a role in the emission of plant volatiles.

Relationship between the heat tolerance of photosynthesis and the thermal stability of rubisco activase in plants from contrasting thermal environments.

Inhibition of net photosynthesis (Pn) by moderate heat stress has been attributed to an inability of Rubisco activase to maintain Rubisco in an active form. To examine this proposal, the temperature response of Pn, Rubisco activation, chlorophyll fluorescence, and the activities of Rubisco and Rubisco activase were examined in species from contrasting environments. The temperature optimum of Rubisco activation was 10 degrees C higher in the creosote bush (Larrea tridentata) compared with the Antarctic hairgrass (Deschampsia antarctica), resembling the temperature response of Pn. Pn increased markedly with increasing internal CO(2) concentration in Antarctic hairgrass and creosote bush plants subjected to moderate heat stress even under nonphotorespiratory conditions. Nonphotochemical quenching of chlorophyll fluorescence, the effective quantum yield of photochemical energy conversion (DeltaF/F(m)') and the maximum yield of PSII (F(v)/F(m)) were more sensitive to temperature in Antarctic hairgrass and two other species endemic to cold regions (i.e. Lysipomia pumila and spinach [Spinacea oleracea]) compared with creosote bush and three species (i.e. jojoba [Simmondsia chinensis], tobacco [Nicotiana tabacum], and cotton [Gossypium hirsutum]) from warm regions. The temperature response of activity and the rate of catalytic inactivation of Rubisco from creosote bush and Antarctic hairgrass were similar, whereas the optimum for ATP hydrolysis and Rubisco activation by recombinant creosote bush, cotton, and tobacco activase was 8 degrees C to 10 degrees C higher than for Antarctic hairgrass and spinach activase. These results support a role for activase in limiting photosynthesis at high temperature.

Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis.

Although the catalytic activity of Rubisco increases with temperature, the low affinity of the enzyme for CO(2) and its dual nature as an oxygenase limit the possible increase in net photosynthesis with temperature. For cotton, comparisons of measured rates of net photosynthesis with predicted rates that take into account limitations imposed by the kinetic properties of Rubisco indicate that direct inhibition of photosynthesis occurs at temperatures higher than about 30 degrees C. Inhibition of photosynthesis by moderate heat stress (i.e. 30-42 degrees C) is generally attributed to reduced rates of RuBP regeneration caused by disruption of electron transport activity, and specifically inactivation of the oxygen evolving enzymes of photosystem II. However, measurements of chlorophyll fluorescence and metabolite levels at air-levels of CO(2) indicate that electron transport activity is not limiting at temperatures that inhibit CO(2) fixation. Instead, recent evidence shows that inhibition of net photosynthesis correlates with a decrease in the activation state of Rubisco in both C(3) and C(4) plants and that this decrease in the amount of active Rubisco can fully account for the temperature response of net photosynthesis. Biochemically, the decrease in Rubisco activation can be attributed to: (1) more rapid de-activation of Rubisco caused by a faster rate of dead-end product formation; and (2) slower re-activation of Rubisco by activase. The net result is that as temperature increases activase becomes less effective in keeping Rubisco catalytically competent. In this opinionated review, we discuss how these processes limit photosynthetic performance under moderate heat stress.

Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants.

Plants are commonly attacked by more than one species of herbivore, potentially causing the induction of multiple, and possibly competing, plant defense systems. In the present paper, we determined the interaction between feeding by the phloem feeder silverleaf whitefly (SWF), Bemisia tabaci Gennadius (B-biotype = B. argentifolii Bellows and Perring), and the leaf-chewing beet armyworm (BAW), Spodoptera exigua Hübner, with regard to the induction of volatile compounds from cotton plants. Compared to undamaged control plants, infestation with SWF did not induce volatile emissions or affect the number and density of pigment glands that store volatile and nonvolatile terpenoid compounds, whereas infestation by BAW strongly induced plant volatile emission. When challenged by the two insect herbivores simultaneously, volatile emission was significantly less than for plants infested with only BAW. Our results suggest that tritrophic level interactions between cotton, BAW, and natural enemies of BAW, that are known to be mediated by plant volatile emissions, may be perturbed by simultaneous infestation by SWF. Possible mechanisms by which the presence of whiteflies may attenuate volatile emissions from caterpillar-damaged cotton plants are discussed.

Lygus hesperus feeding and salivary gland extracts induce volatile emissions in plants.

Induction of plant volatiles by leaf-chewing caterpillars is well documented. However, there is much less information about volatile induction by insects with different feeding habits. We studied the induction of plant volatiles by a piercing-sucking insect, the western tarnished plant bug Lygus hesperus Knight. Adults of both genders and nymphs of Lygus induced the local emission of a blend of volatiles from both cotton and maize. Feeding by Lygus also induced the systemic emission of volatiles that was similar but less complex than the blend emitted at the site of feeding. Infestation by mated, mature adult females (>4 days old), but not by nymphs or mature males, caused detectable emission of alpha-pinene, myrcene. and (E)-beta-caryophyllene, compounds that are stored in the glands of cotton tissue. This indicated that damage to glands in the petiole and leaf by the female ovipositor, rather than feeding, contributed significantly to the emission of these volatiles. Girdling the plant stem to disrupt phloem transport markedly decreased the movement of 14C-labeled photosynthetic products to the apex of the plant, and this treatment also markedly reduced the amount of systemically induced volatiles caused by Lygus feeding. Lygus salivary gland extracts were capable of inducing emission of the same volatile blend as measured for plants infested by feeding insects or treated with volicitin. an elicitor isolated from caterpillar regurgitant. The results indicate that L. hesperus is capable of inducing the emission of plant volatiles and that induction is caused by an elicitor that is contained in the insect salivary gland.

Sensitivity of photosynthesis in a C4 plant, maize, to heat stress.

Our objective was to determine the sensitivity of components of the photosynthetic apparatus of maize (Zea mays), a C4 plant, to high temperature stress. Net photosynthesis (Pn) was inhibited at leaf temperatures above 38 degrees C, and the inhibition was much more severe when the temperature was increased rapidly rather than gradually. Transpiration rate increased progressively with leaf temperature, indicating that inhibition was not associated with stomatal closure. Nonphotochemical fluorescence quenching (qN) increased at leaf temperatures above 30 degrees C, indicating increased thylakoid energization even at temperatures that did not inhibit Pn. Compared with CO(2) assimilation, the maximum quantum yield of photosystem II (F(v)/F(m)) was relatively insensitive to leaf temperatures up to 45 degrees C. The activation state of phosphoenolpyruvate carboxylase decreased marginally at leaf temperatures above 40 degrees C, and the activity of pyruvate phosphate dikinase was insensitive to temperature up to 45 degrees C. The activation state of Rubisco decreased at temperatures exceeding 32.5 degrees C, with nearly complete inactivation at 45 degrees C. Levels of 3-phosphoglyceric acid and ribulose-1,5-bisphosphate decreased and increased, respectively, as leaf temperature increased, consistent with the decrease in Rubisco activation. When leaf temperature was increased gradually, Rubisco activation acclimated in a similar manner as Pn, and acclimation was associated with the expression of a new activase polypeptide. Rates of Pn calculated solely from the kinetics of Rubisco were remarkably similar to measured rates if the calculation included adjustment for temperature effects on Rubisco activation. We conclude that inactivation of Rubisco was the primary constraint on the rate of Pn of maize leaves as leaf temperature increased above 30 degrees C.