Throwing shade: Limitations to photosynthesis at high planting densities and how to overcome them

Photosynthesis underpins plant productivity but is highly sensitive to changes in the environment; particularly that of light. Light fluctuations can occur over different timescales and pose a complex challenge for the photosynthetic machinery, with the need for efficient capture and simultaneous mitigation of any damage caused by excess light energy (Demmig-Adams et al., 2012; Durand et al., 2021). Several pathways determine the exact response of photosynthesis, including the induction state of photosynthetic enzymes, induction and relaxation of energy dissipation pathways, stomatal aperture, and the acclimation state of the leaf (Walters, 2004; Zhu et al., 2010; Ruban, 2017; Matthews et al., 2018). Differences within these pathways affect biomass production and yield, thus providing potential targets for increasing crop yields (Kromdijk et al., 2016; Acevedo-Siaca et al., 2020).

Within crop canopies, environmental conditions combined with agronomy and management determine the exact light environment to which plants, and individual leaves, are exposed. In the field, the baseline maximum light intensity for photosynthesis on a fully sunny day depends upon solar movement, with a steady increase up to a peak at solar noon followed by a decrease (Figure 1; black line). The available light intensity for each section of the plant and the leaf will then depend upon features including cloud cover, planting density, wind-induced crop movement, canopy structure, and position in the canopy (Figure 1; colored lines; Townsend et al., 2018; Wang et al., 2020; Durand et al., 2021). This results in transient decreases in available light intensity and corresponding spectral composition (i.e. the wavelengths of light available), where the magnitude, duration, and frequency of which depend upon all features combined.

Figure 1.

Example diurnal changes in photosynthetically active radiation (PAR: 400–700 nm) according to leaf position available for photosynthesis on a fully sunny day (adapted from Townsend et al., 2018). The black line indicates PAR above a modeled (wheat [Triticum aestivum L.]) canopy and the colored lines indicate positions within the canopy where increasing canopy depth results in a progressive decrease in total PAR and a reduction in the frequency and duration of high light events (i.e. from red to green to blue).

Increasing plant density (e.g. growing more plants per unit area) constitutes a common approach to achieving higher productivity in agriculture. Specifically for maize (Zea mays L.), planting density has increased from 30,000 to over 80,000 plants ha⁻¹ in the past decades, which has been responsible for a tremendous increase in yield gains (Duvick, 2005). Growing plants at a higher density, however, decreases biomass and yield per plant due to competition for water, nutrients, and especially light (Postma et al., 2021). To mitigate light competition in dense planting settings, maize breeders have selected modern hybrids with more upright leaves, which allow a more homogeneous vertical light distribution throughout the canopy and sustains light capture and photosynthesis on the leaves surrounding the ear position (Lacasa et al., 2022). In spite of the large improvements associated with modern maize hybrids, increased planting density still limits the light intensity that leaves intercept as well as more frequent light fluctuations.

Within this issue of Plant Physiology, Wu et al. (2022) conducted field experiments on maize with three different planting densities (15,000, 75,000, and 135,000 plants ha⁻¹) to understand which aspects of the light environment impact the photosynthetic mechanism of crop yield. Increases in planting density from 15,000 to 135,000 plants ha⁻¹ significantly decreased both maximum (from 2,200 to 1,300 μmol m⁻² s⁻¹) and minimum (from 80 to 50 μmol m⁻² s⁻¹; Figure 2) light intensities as well as increased light fluctuation frequency by 15 times. The maximum increase in planting density also shortened the duration of plant exposure to high light and increased the exposure to low light (below 200 μmol m⁻² s⁻¹). Altogether, these changes in the light environment translated into changes in photosynthetic performance and yield at the individual plant level as well as the whole system level. Overall, individuals planted at the highest density achieved lower photosynthetic rates compared with individuals at the lowest planting densities. They also experienced much more abrupt changes in the photosynthetic rates throughout the day, with a greater proportion of time spent operating at very low photosynthetic rates. The impairments in photosynthesis under the highest planting density were a result of both the direct impact of a lower daily high light duration and also the indirect impact of the formation of shade-adapted leaves. These shade-adapted leaves performed better at lower light at the cost of lower maximum photosynthetic rates and slower induction of photosynthesis.

Figure 2.

Effect of planting density on yield and biomass. Values are shown per (A) unit area and (B) plant. Redrawn from Wu et al. (2022). Data are mean ± SD (n = 10). Different letters indicate differences between densities (P < 0.05, least significant difference test). HD, high planting density (135,000 plants ha⁻¹); LD, low planting density (15,000 plants ha⁻¹); MD, medium planting density (75,000 plants ha⁻¹).

Wu et al. (2022) also performed experiments on maize plants under controlled conditions to simulate different durations of high light exposure as well as different frequencies of light fluctuations between high and low irradiance levels. These simulations demonstrated that reductions in the duration of high light have a greater impact on photosynthesis than an increased frequency of fluctuations. However, under field conditions, the more frequent fluctuations in light intensity at dense plantings considerably reduced the duration of high light and most importantly the duration of maximum photosynthesis at high light. Maximum photosynthesis for a given light intensity is not instantaneously achieved upon light exposure. In fact, there is often a lag between the change in light intensity and the photosynthetic response, which is dictated by the speed of photosynthetic induction and the speed of stomatal opening (Retkute et al., 2015; Matthews et al., 2018). Therefore, it is difficult to disentangle the impact of light fluctuation frequency from that of the duration of high light on plant function, and it is possible that a combination of these two factors results in lower photosynthesis and carbon gain loss under field conditions. This would correspond with the findings of Retkute et al. (2015), who found that both the fraction of time spent under low versus high irradiance as well as the frequency of switches contribute to overall photosynthetic performance in Arabidopsis (Arabidopsis thaliana).

As a result of the lower light and photosynthesis, Wu et al. (2022) observed lower biomass and ear weight per plant at high planting densities, with a strong positive association between biomass and yield per plant with light intensity and photosynthesis. Biomass and yield per unit area, however, were two and three times higher at the highest planting density compared with that of the mid and lowest planting densities, respectively. It is important to highlight that increases in biomass and yield per unit area were much greater between the two lower planting densities (15,000 and 75,000 plants ha⁻¹) relative to the two higher planting densities (75,000 and 135,000 plants ha⁻¹). This indicates that increasing the planting densities above a threshold is neither efficient nor profitable given the high plant–plant competition for a number of resources, with light likely being an important limiting factor (Hashemi-Dezfouli and Herbert, 1992; Postma et al., 2021).

An ideal solution to improving maize yield would entail generating hybrids that could achieve high yield at the individual level under denser plantings (>75,000 plants ha⁻¹). This could be achieved through introducing traits that optimize canopy architecture to permit greater light attenuation (Tian et al., 2019). Similar to other cereal crops, erect leaf stature continues to be cited as a potential beneficial trait in maize. Tian et al. (2019) characterized an allele that reduces leaf angle in the wild ancestor of maize (i.e. teosinte; Zea sp.) that was lost during maize domestication. They demonstrated that introgressing this wild allele into modern hybrids allows for increased yield under high-density plantings. Other optimized canopy traits may include slight decreases in leaf area per plant to reduce mutual leaf shading (Liu et al., 2022). Alternatively, an increased speed of response to fluctuating light environments, for example with improved induction rates or faster stomatal movement (Horaruang et al., 2022), could provide a biochemical alternative. Further studies in this direction might constitute an interesting approach to improving plant productivity at dense plantings, especially considering the decreases in the amount of solar radiation reaching the Earth's surface in recent decades.