Mechanism of growth inhibition mediated by disorder of chlorophyll metabolism in rice (Oryza sativa) under the stress of three polycyclic aromatic hydrocarbons

Abstract

Photosynthesis mediated by chlorophyll metabolism is the basis for plant growth, and also the important regulatory mechanism of carbon pool in cropland ecosystems. Soil organic pollutants induced growth inhibition in crop plants, herein, we conducted an in-depth investigation on the effects of three representative polycyclic aromatic hydrocarbons (PAHs), including phenanthrene (PHE), pyrene (PYR), and benzo[a]pyrene (BaP) on rice (Oryza sativa) growth and photosynthesis. PAHs were absorbed via root uptake and accumulated in leaves, causing the swelling of thylakoids and the increase of osmiophilic granules in chloroplasts. The actual quantum efficiency of PSII was significantly decreased under the stress of PHE, PYR, and BaP by 29.9%, 11.9%, and 24.1% respectively, indicating the inhibition in photon absorption and transfer, which was consistent with the decrease of chlorophyll a (22.3%–32.2% compared to the control) in rice leaves. Twenty-two encoding genes involved in chlorophyll metabolism were determined and the results indicated that the expression of chlorophyll synthetases was downregulated by over 50% whereas the degradation process was promoted. Consequently, the production of carbohydrates and the carbon fixation were inhibited, which revealed by the downregulation of intermediate metabolites in Calvin cycle and the declined carboxylation rate. The disturbed photosynthesis resulted in the decrease of the biomasses of both roots (21.0%–42.7%) and leaves (6.4%–22.1%) under the tested PAH stresses. The findings of this study implied that the photosynthetic inhibition was possibly attributed to the disorder of chlorophyll metabolism, thus providing novel insights into the mechanism of growth inhibition induced by organic pollutants and theoretical basis for the estimation of cropland carbon sequestration potential.