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Fulltext Photoprotection as a Trait for Rice Yield Improvement: Status and Prospects

Murchie EH, Ali A, Herman T

Rice (N Y), 2015 Dec;8(1):31.
PMID: 26424004 DOI: 10.1186/s12284-015-0065-2

Solar radiation is essential for photosynthesis and global crop productivity but it is also variable in space and time, frequently being limiting or in excess of plant requirements depending on season, environment and microclimate. Photoprotective mechanisms at the chloroplast level help to avoid oxidative stress and photoinhibition, which is a light-induced reduction in photosynthetic quantum efficiency often caused by damage to photosystem II. There is convincing evidence that photoinhibition has a large impact on biomass production in crops and this may be especially high in rice, which is typically exposed to high tropical light levels. Thus far there has been little attention to photoinhibition as a target for improvement of crop yield. However, we now have sufficient evidence to examine avenues for alleviation of this particular stress and the physiological and genetic basis for improvement in rice and other crops. Here we examine this evidence and identify new areas for attention. In particular we discuss how photoprotective mechanisms must be optimised at both the molecular and the canopy level in order to coordinate with efficient photosynthetic regulation and realise an increased biomass and yield in rice.
Fulltext Exploring Relationships between Canopy Architecture, Light Distribution, and Photosynthesis in Contrasting Rice Genotypes Using 3D Canopy Reconstruction

Burgess AJ, Retkute R, Herman T, Murchie EH

Front Plant Sci, 2017;8:734.
PMID: 28567045 DOI: 10.3389/fpls.2017.00734

The arrangement of leaf material is critical in determining the light environment, and subsequently the photosynthetic productivity of complex crop canopies. However, links between specific canopy architectural traits and photosynthetic productivity across a wide genetic background are poorly understood for field grown crops. The architecture of five genetically diverse rice varieties-four parental founders of a multi-parent advanced generation intercross (MAGIC) population plus a high yielding Philippine variety (IR64)-was captured at two different growth stages using a method for digital plant reconstruction based on stereocameras. Ray tracing was employed to explore the effects of canopy architecture on the resulting light environment in high-resolution, whilst gas exchange measurements were combined with an empirical model of photosynthesis to calculate an estimated carbon gain and total light interception. To further test the impact of different dynamic light patterns on photosynthetic properties, an empirical model of photosynthetic acclimation was employed to predict the optimal light-saturated photosynthesis rate (Pmax ) throughout canopy depth, hypothesizing that light is the sole determinant of productivity in these conditions. First, we show that a plant type with steeper leaf angles allows more efficient penetration of light into lower canopy layers and this, in turn, leads to a greater photosynthetic potential. Second the predicted optimal Pmax responds in a manner that is consistent with fractional interception and leaf area index across this germplasm. However, measured Pmax , especially in lower layers, was consistently higher than the optimal Pmax indicating factors other than light determine photosynthesis profiles. Lastly, varieties with more upright architecture exhibit higher maximum quantum yield of photosynthesis indicating a canopy-level impact on photosynthetic efficiency.
Fulltext A multiscale mathematical model describing the growth and development of bambara groundnut

Dodd J, Sweby PK, Mayes S, Murchie EH, Karunaratne AS, Massawe F, et al.

J Theor Biol, 2023 Mar 07;560:111373.
PMID: 36509139 DOI: 10.1016/j.jtbi.2022.111373

A principal objective in agriculture is to maximise food production; this is particularly relevant with the added demands of an ever increasing population, coupled with the unpredictability that climate change brings. Further improvements in productivity can only be achieved with an increased understanding of plant and crop processes. In this respect, mathematical modelling of plants and crops plays an important role. In this paper we present a two-scale mathematical model of crop yield that accounts for plant growth and canopy interactions. A system of nonlinear ordinary differential equations (ODEs) is formulated to describe the growth of each individual plant, where equations are coupled via a term that describes plant competition via canopy-canopy interactions. A crop of greenhouse plants is then modelled via an agent based modelling approach in which the growth of each plant is described via our system of ODEs. The model is formulated for the African drought tolerant legume bambara groundnut (Vigna subterranea), which is currently being investigated as a food source in light of climate change and food insecurity challenges. Our model allows us to account for plant diversity and also investigate the effect of individual plant traits (e.g. plant canopy size and planting distance) on the yield of the overall crop. Informed with greenhouse data, model results show that plant positioning relative to other plants has a large impact on individual plant yield. Variation in physiological plant traits from genetic diversity and the environmental effects lead to experimentally observed variations in crop yield. These traits include plant height, plant carrying capacity, leaf accumulation rate and canopy spread. Of these traits plant height and ground cover growth rates are found to have the greatest impact on crop yield. We also consider a range of different planting arrangements (uniform grid, staggered grid, circular rings and random allocation) and find that the staggered grid leads to the greatest crop yield (6% more compared to uniform grid). Whilst formulated specifically for bambara groundnut, the generic formulation of our model means that with changes to certain parameter's, it may be extended to other crop species that form a canopy.
The 4-Dimensional Plant: Effects of Wind-Induced Canopy Movement on Light Fluctuations and Photosynthesis

Burgess AJ, Retkute R, Preston SP, Jensen OE, Pound MP, Pridmore TP, et al.

Front Plant Sci, 2016;7:1392.
PMID: 27708654

Physical perturbation of a plant canopy brought about by wind is a ubiquitous phenomenon and yet its biological importance has often been overlooked. This is partly due to the complexity of the issue at hand: wind-induced movement (or mechanical excitation) is a stochastic process which is difficult to measure and quantify; plant motion is dependent upon canopy architectural features which, until recently, were difficult to accurately represent and model in 3-dimensions; light patterning throughout a canopy is difficult to compute at high-resolutions, especially when confounded by other environmental variables. Recent studies have reinforced the expectation that canopy architecture is a strong determinant of productivity and yield; however, links between the architectural properties of the plant and its mechanical properties, particularly its response to wind, are relatively unknown. As a result, biologically relevant data relating canopy architecture, light- dynamics, and short-scale photosynthetic responses in the canopy setting are scarce. Here, we hypothesize that wind-induced movement will have large consequences for the photosynthetic productivity of our crops due to its influence on light patterning. To address this issue, in this study we combined high resolution 3D reconstructions of a plant canopy with a simple representation of canopy perturbation as a result of wind using solid body rotation in order to explore the potential effects on light patterning, interception, and photosynthetic productivity. We looked at two different scenarios: firstly a constant distortion where a rice canopy was subject to a permanent distortion throughout the whole day; and secondly, a dynamic distortion, where the canopy was distorted in incremental steps between two extremes at set time points in the day. We find that mechanical canopy excitation substantially alters light dynamics; light distribution and modeled canopy carbon gain. We then discuss methods required for accurate modeling of mechanical canopy excitation (here coined the 4-dimensional plant) and some associated biological and applied implications of such techniques. We hypothesize that biomechanical plant properties are a specific adaptation to achieve wind-induced photosynthetic enhancement and we outline how traits facilitating canopy excitation could be used as a route for improving crop yield.
Fulltext Image-based 3D canopy reconstruction to determine potential productivity in complex multi-species crop systems

Burgess AJ, Retkute R, Pound MP, Mayes S, Murchie EH

Ann Bot, 2017 Mar 01;119(4):517-532.
PMID: 28065926 DOI: 10.1093/aob/mcw242

BACKGROUND AND AIMS: Intercropping systems contain two or more species simultaneously in close proximity. Due to contrasting features of the component crops, quantification of the light environment and photosynthetic productivity is extremely difficult. However it is an essential component of productivity. Here, a low-tech but high-resolution method is presented that can be applied to single- and multi-species cropping systems to facilitate characterization of the light environment. Different row layouts of an intercrop consisting of Bambara groundnut ( Vigna subterranea ) and proso millet ( Panicum miliaceum ) have been used as an example and the new opportunities presented by this approach have been analysed.
METHODS: Three-dimensional plant reconstruction, based on stereo cameras, combined with ray tracing was implemented to explore the light environment within the Bambara groundnut-proso millet intercropping system and associated monocrops. Gas exchange data were used to predict the total carbon gain of each component crop.
KEY RESULTS: The shading influence of the tall proso millet on the shorter Bambara groundnut results in a reduction in total canopy light interception and carbon gain. However, the increased leaf area index (LAI) of proso millet, higher photosynthetic potential due to the C4 pathway and sub-optimal photosynthetic acclimation of Bambara groundnut to shade means that increasing the number of rows of millet will lead to greater light interception and carbon gain per unit ground area, despite Bambara groundnut intercepting more light per unit leaf area.
CONCLUSIONS: Three-dimensional reconstruction combined with ray tracing provides a novel, accurate method of exploring the light environment within an intercrop that does not require difficult measurements of light interception and data-intensive manual reconstruction, especially for such systems with inherently high spatial possibilities. It provides new opportunities for calculating potential productivity within multi-species cropping systems, enables the quantification of dynamic physiological differences between crops grown as monoculture and those within intercrops, and enables the prediction of new productive combinations of previously untested crops.
Fulltext Suboptimal Acclimation of Photosynthesis to Light in Wheat Canopies

Townsend AJ, Retkute R, Chinnathambi K, Randall JWP, Foulkes J, Carmo-Silva E, et al.

Plant Physiol, 2018 Feb;176(2):1233-1246.
PMID: 29217593 DOI: 10.1104/pp.17.01213

Photosynthetic acclimation (photoacclimation) is the process whereby leaves alter their morphology and/or biochemistry to optimize photosynthetic efficiency and productivity according to long-term changes in the light environment. The three-dimensional architecture of plant canopies imposes complex light dynamics, but the drivers for photoacclimation in such fluctuating environments are poorly understood. A technique for high-resolution three-dimensional reconstruction was combined with ray tracing to simulate a daily time course of radiation profiles for architecturally contrasting field-grown wheat (Triticum aestivum) canopies. An empirical model of photoacclimation was adapted to predict the optimal distribution of photosynthesis according to the fluctuating light patterns throughout the canopies. While the photoacclimation model output showed good correlation with field-measured gas-exchange data at the top of the canopy, it predicted a lower optimal light-saturated rate of photosynthesis at the base. Leaf Rubisco and protein contents were consistent with the measured optimal light-saturated rate of photosynthesis. We conclude that, although the photosynthetic capacity of leaves is high enough to exploit brief periods of high light within the canopy (particularly toward the base), the frequency and duration of such sunflecks are too small to make acclimation a viable strategy in terms of carbon gain. This suboptimal acclimation renders a large portion of residual photosynthetic capacity unused and reduces photosynthetic nitrogen use efficiency at the canopy level, with further implications for photosynthetic productivity. It is argued that (1) this represents an untapped source of photosynthetic potential and (2) canopy nitrogen could be lowered with no detriment to carbon gain or grain protein content.
Fulltext Increasing leaf vein density by mutagenesis: laying the foundations for C4 rice

Feldman AB, Murchie EH, Leung H, Baraoidan M, Coe R, Yu SM, et al.

PLoS One, 2014;9(4):e94947.
PMID: 24760084 DOI: 10.1371/journal.pone.0094947

A high leaf vein density is both an essential feature of C4 photosynthesis and a foundation trait to C4 evolution, ensuring the optimal proportion and proximity of mesophyll and bundle sheath cells for permitting the rapid exchange of photosynthates. Two rice mutant populations, a deletion mutant library with a cv. IR64 background (12,470 lines) and a T-DNA insertion mutant library with a cv. Tainung 67 background (10,830 lines), were screened for increases in vein density. A high throughput method with handheld microscopes was developed and its accuracy was supported by more rigorous microscopy analysis. Eight lines with significantly increased leaf vein densities were identified to be used as genetic stock for the global C4 Rice Consortium. The candidate population was shown to include both shared and independent mutations and so more than one gene controlled the high vein density phenotype. The high vein density trait was found to be linked to a narrow leaf width trait but the linkage was incomplete. The more genetically robust narrow leaf width trait was proposed to be used as a reliable phenotypic marker for finding high vein density variants in rice in future screens.
Fulltext Increasing Leaf Vein Density via Mutagenesis in Rice Results in an Enhanced Rate of Photosynthesis, Smaller Cell Sizes and Can Reduce Interveinal Mesophyll Cell Number

Feldman AB, Leung H, Baraoidan M, Elmido-Mabilangan A, Canicosa I, Quick WP, et al.

Front Plant Sci, 2017;8:1883.
PMID: 29163607 DOI: 10.3389/fpls.2017.01883

Improvements to leaf photosynthetic rates of crops can be achieved by targeted manipulation of individual component processes, such as the activity and properties of RuBisCO or photoprotection. This study shows that simple forward genetic screens of mutant populations can also be used to rapidly generate photosynthesis variants that are useful for breeding. Increasing leaf vein density (concentration of vascular tissue per unit leaf area) has important implications for plant hydraulic properties and assimilate transport. It was an important step to improving photosynthetic rates in the evolution of both C3 and C4 species and is a foundation or prerequisite trait for C4 engineering in crops like rice (Oryza sativa). A previous high throughput screen identified five mutant rice lines (cv. IR64) with increased vein densities and associated narrower leaf widths (Feldman et al., 2014). Here, these high vein density rice variants were analyzed for properties related to photosynthesis. Two lines were identified as having significantly reduced mesophyll to bundle sheath cell number ratios. All five lines had 20% higher light saturated photosynthetic capacity per unit leaf area, higher maximum carboxylation rates, dark respiration rates and electron transport capacities. This was associated with no significant differences in leaf thickness, stomatal conductance or CO2 compensation point between mutants and the wild-type. The enhanced photosynthetic rate in these lines may be a result of increased RuBisCO and electron transport component amount and/or activity and/or enhanced transport of photoassimilates. We conclude that high vein density (associated with altered mesophyll cell length and number) is a trait that may confer increased photosynthetic efficiency without increased transpiration.