Acclimation of C4 metabolism to low light in mature maize leaves could limit energetic losses during progressive shading in a crop canopy

Abstract

C4 plants have a biochemical carbon-concentrating mechanism that increases CO2 concentration around Rubisco in the bundle sheath. Under low light, the activity of the carbon-concentrating mechanism generally decreases, associated with an increase in leakiness (ϕ), the ratio of CO2 retrodiffusing from the bundle sheath relative to C4 carboxylation. This increase in ϕ had been theoretically associated with a decrease in biochemical operating efficiency (expressed as ATP cost of gross assimilation, ATP/GA) under low light and, because a proportion of canopy photosynthesis is carried out by shaded leaves, potential productivity losses at field scale. Maize plants were grown under light regimes representing the cycle that leaves undergo in the canopy, whereby younger leaves initially developed under high light and were then re-acclimated to low light (600 to 100 μE·m−2·s−1 photosynthetically active radiation) for 3 weeks. Following re-acclimation, leaves reduced rates of light-respiration and reached a status of lower ϕ, effectively optimizing the limited ATP resources available under low photosynthetically active radiation. Direct estimates of respiration in the light, and ATP production rate, allowed an empirical estimate of ATP production rate relative to gross assimilation to be derived. These values were compared to modelled ATP/GA which was predicted using leakiness as the sole proxy for ATP/GA, and, using a novel comprehensive biochemical model, showing that irrespective of whether leaves are acclimated to very low or high light intensity, the biochemical efficiency of the C4 cycle does not decrease at low photosynthetically active radiation.

A high throughput gas exchange screen for determining rates of photorespiration or regulation of C4 activity

“…For instance, in Cocklebur ( Xanthium strumarium L., Asteraceae), R LIGHT was significantly different from dark respiration (Tcherkez et al , 2008), whereas in maize R LIGHT is generally non-significantly different from dark respiration (C. Bellasio, unpublished data). The most suitable method to estimate R LIGHT should therefore be evaluated on a case-by-case basis (see Bellasio and Griffiths, 2014a), and for a uniform population (e.g. one species or set of transformants in a growth chamber), R LIGHT could be estimated on a subset of individuals, with one of the methods described above.…”

An Excel tool for deriving key photosynthetic parameters from combined gas exchange and chlorophyll fluorescence: theory and practice

“…), and represents the capacity of crops to perform well under limited light (Yongjian et al . 1998; Craine & Reich ; Bellasio & Griffiths ). Stress events affecting respiration or the photosynthetic capacity will readily be mirrored by the LCP .…”

“…If a value for R LIGHT is available, sheets 5a and 5b calculate the C i – GA compensation point C i * (also referred to as the CO 2 compensation point in absence of R LIGHT ). C i * is a useful proxy in comparative studies, having the advantage over Γ of not being susceptible to variability in R LIGHT which responds readily to environmental conditions (Buckley & Adams ; Bellasio & Griffiths 2014a,b). C i * is solved in sheets 5a and 5b as the x ‐value of the fitted Eqn in correspondence with A MOD = − R LIGHT (Ethier & Livingston ), similar to Eqn .…”

“…Both the Valentini calibration (Gilbert et al . ) and the Yin calibration (Bellasio & Griffiths ) were modified to account for non‐linearity, and here we implemented the simple approach presented by Bellasio (Bellasio & Griffiths 2014a,b) in the experimentally validated C 3 version (Bellasio et al . ).…”

Insights into C 4 metabolism from comparative deep sequencing

“…RNA-seq has been used to report mRNA signatures associated with the 'NAD-ME', 'NADP-ME' or 'PEPCK' biochemical subtypes [11,12 ,13], and along with theoretical and modelling approaches, has provided clear evidence that often two of the decarboxylases operate in parallel, with their relative contributions varying depending on conditions [14][15][16][17]. However, our understanding of what changes leaf anatomy such that contact between tissues involved in carbon assimilation and reduction is increased (Figure 1a), and also what sets up and then maintains the patterns of gene expression required for the C 4 cycle are rudimentary.…”