Importance of the green color, absorption gradient, and spectral absorption of chloroplasts for the radiative energy balance of leaves

Abstract

Terrestrial green plants absorb photosynthetically active radiation (PAR; 400-700 nm) but do not absorb photons evenly across the PAR waveband. The spectral absorbance of photosystems and chloroplasts is lowest for green light, which occurs within the highest irradiance waveband of direct solar radiation. We demonstrate a close relationship between this phenomenon and the safe and efficient utilization of direct solar radiation in simple biophysiological models. The effects of spectral absorptance on the photon and irradiance absorption processes are evaluated using the spectra of direct and diffuse solar radiation. The radiation absorption of a leaf arises as a consequence of the absorption of chloroplasts. The photon absorption of chloroplasts is strongly dependent on the distribution of pigment concentrations and their absorbance spectra. While chloroplast movements in response to light are important mechanisms controlling PAR absorption, they are not effective for green light because chloroplasts have the lowest spectral absorptance in the waveband. With the development of palisade tissue, the incident photons per total palisade cell surface area and the absorbed photons per chloroplast decrease. The spectral absorbance of carotenoids is effective in eliminating shortwave PAR (<520 nm), which contains much of the surplus energy that is not used for photosynthesis and is dissipated as heat. The PAR absorptance of a whole leaf shows no substantial difference based on the spectra of direct or diffuse solar radiation. However, most of the near infrared radiation is unabsorbed and heat stress is greatly reduced. The incident solar radiation is too strong to be utilized for photosynthesis under the current CO₂ concentration in the terrestrial environment. Therefore, the photon absorption of a whole leaf is efficiently regulated by photosynthetic pigments with low spectral absorptance in the highest irradiance waveband and through a combination of pigment density distribution and leaf anatomical structures.

Keywords: Absorption spectra; Carotenoids; Chloroplast movement; Direct radiation; Palisade tissue; Photosystem.

Fig. 1

An example of spectral irradiance and photon flux density (PFD) measured on a clear day (day of year = 195) in 2011 at noon (36.05°N, 140.12°E). Measurements were conducted at 1-min intervals averaged over 1 h (11:30 am to 12:30 pm). a Spectral irradiance and PFD of global solar radiation. Surplus energy for photosynthesis (Es) is also shown (see the main text). b Spectral irradiance of direct (dark line) and diffuse radiation (light line). c Spectral PFD of direct (dark line) and diffuse radiation (light line) (Adapted from Kume et al. 2016)

Fig. 2

Relationships between spectral irradiance of direct solar PAR at noon and (a) spectral absorbance of purified LHCII trimer and PSI-LHCI and (b) spectral absorbance of an Ulva thallus and the leaves of Oryza and Quercus (Kume et al. 2016). The graphs are plotted with spectral absorbance on the y-axis and the spectral irradiance on the x-axis at 3.35-nm intervals in the 400- to 680-nm bandwidth. Points with consecutive wavelengths are connected with a line. The points with the shortest (400 nm) and longest wavelengths (680 nm) are indicated by a square and a cross, respectively

Fig. 3

Absorptance spectra of the LHCII trimer (Hogewoning et al. 2012), β-carotene (Lichtenthaler 1987), a green alga thallus (Ulva taeniata) (Haxo and Blinks 1950), a grass leaf (Oryza sativa) and a tree leaf (Quercus crispula) (Noda et al. 2014). The absorptance of the LHCII trimer is adjusted to 0.3 for PAR and that of β-carotene is adjusted to 0.2 for PAR

Fig. 4

Model explaining the energy absorption of a chloroplast-like absorber with a different molecular absorption coefficient and position. The size of the absorber is 5 μm × 5 μm × 2 μm; the projected area of the short axis is 25 μm², and the area of the long axis is 10 μm². It is assumed that a 400 W m⁻² of beam of incident radiation reaches the absorber

Fig. 5

Model explaining the energy balance of a series of three chloroplasts with the same absorptance. Left: cuvettes containing a green pigment solution with the same spectral absorptance as that of LHCII. Right: cuvettes containing a gray solution. Both colored cuvettes have 0.3 of PAR absorptance (see Fig. 6a). Incident beam PAR radiation has the same spectral properties as the global solar radiation at noon (Fig. 1) and is 400 W m⁻² of irradiance or 2,000 μmol m⁻² s⁻¹ of PFD (values in parentheses)

Fig. 6

a Spectral absorptance of the gray body (dashed line) and simplified green chloroplast (solid line). In both cases, the mean PAR absorptance is 0.3. b Changes in spectral irradiance by the absorption of three green chloroplasts. The ratio of green light components exponentially increased at each absorption step

Fig. 7

Model explaining the energy balance of a series of three chloroplasts with absorptance gradient. Left: cuvettes containing a green pigment solution with the same spectral absorptance as LHCII. Right: cuvettes containing a gray solution. The colored cuvettes have 0.15, 0.20, and 0.25 PAR absorptance from top to bottom, respectively. The incident beam PAR radiation has the same spectral properties as the global solar radiation at noon (Fig. 1), with 400 W m⁻² of irradiance or 2000 μmol m⁻² s⁻¹ of PFD (values in parenthesis are for PFD)

Fig. 8

Model explaining the effects of the aspect ratio of palisade cells (cell length per column diameter) on the absorption areas of chloroplasts. The effective absorption area increases with the aspect ratio. Therefore, the absorption of photons of direct radiation per chloroplast is nearly inversely proportional to the aspect ratio. The stacked palisade cells with the absorptance gradient in chloroplasts (the right end) can absorb photons more efficiently

Fig. 9

Effects of pigment concentration on changes in the profile of absorptance spectra. a Profiles of the spectral absorptance of LHCII with different mean PAR absorptance values (mean PAR absorptance). The spectra were normalized to the maxima of the Soret bands. In real leaves, multiple absorptions within leaf tissues decrease the absorption depression in the green region (detour effect). b The ratio of the absorptance of LHCII (α_LHCII) to that of the gray absorber with the same absorptance (α_Gray) under different radiation classes (global, direct and diffuse; solar irradiance and photons; see Fig. 1). The suffix “–G” indicates global radiation, “–Dir” indicates direct radiation and “–Diff” indicates diffuse radiation

Fig. 10

Absorption spectra of β-carotene with 0.2 of PAR absorptance (no units) and energy spectra of surplus energy for photosynthesis (Es) (W m⁻² nm⁻¹). Es was calculated from Eq. (5) (see also Fig. 1a)