Abstract

BackgroundCrassulacean acid metabolism (CAM), a specialized mode of photosynthesis, enables plant adaptation to water-limited environments and improves photosynthetic efficiency via an inorganic carbon-concentrating mechanism. Kalanchoë fedtschenkoi is an obligate CAM model featuring a relatively small genome and easy stable transformation. However, the molecular responses to light quality and intensity in CAM plants remain understudied.ResultsHere we present a genome-wide expression atlas of K. fedtschenkoi plants grown under 12 h/12 h photoperiod with different light quality (blue, red, far-red, white light) and intensity (0, 150, 440, and 1,000 μmol m–2 s–1) based on RNA sequencing performed for mature leaf samples collected at dawn (2 h before the light period) and dusk (2 h before the dark period). An eFP web browser was created for easy access of the gene expression data. Based on the expression atlas, we constructed a light-responsive co-expression network to reveal the potential regulatory relationships in K. fedtschenkoi. Measurements of leaf titratable acidity, soluble sugar, and starch turnover provided metabolic indicators of the magnitude of CAM under the different light treatments and were used to provide biological context for the expression dataset. Furthermore, CAM-related subnetworks were highlighted to showcase genes relevant to CAM pathway, circadian clock, and stomatal movement. In comparison with white light, monochrome blue/red/far-red light treatments repressed the expression of several CAM-related genes at dusk, along with a major reduction in acid accumulation. Increasing light intensity from an intermediate level (440 μmol m−2 s−1) of white light to a high light treatment (1,000 μmol m–2 s–1) increased expression of several genes involved in dark CO2 fixation and malate transport at dawn, along with an increase in organic acid accumulation.ConclusionsThis study provides a useful genomics resource for investigating the molecular mechanism underlying the light regulation of physiology and metabolism in CAM plants. Our results support the hypothesis that both light intensity and light quality can modulate the CAM pathway through regulation of CAM-related genes in K. fedtschenkoi.

Highlights

  • Crassulacean acid metabolism (CAM), a specialized mode of photosynthesis, enables plant adaptation to water-limited environments and improves photosynthetic efficiency via an inorganic carbon-concentrating mechanism

  • When comparing the common differentially expressed gene (DEG) in different light quality or light intensity at dawn and dusk separately (Fig. 2f), we found that the “generation of precursor metabolites and energy” term was enriched in all 4 common DEG sets of different light quality and light intensity at both dawn and dusk

  • Light quality effects at the metabolic and molecular levels have been studied in several plant species [30,31,32,33,34], genome-wide transcriptomic studies of the effects of light quality and light intensity on CAM species are lacking

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Summary

Background

Sunlight is a critical energy resource for plant growth and development, and it functions as an important input signal for the circadian clock, stomatal movement, and photosynthesis pathway. For condition-specific DEGs at different time points or different light conditions, the “photosynthesis” term was strongly enriched in dusk vs dawn DEGs in RL-specific and HL-specific from the light quality comparison and light intensity comparison, respectively (Fig. 2g) This indicates that RL and HL significantly affected photosynthesis-related changes in transcript abundance between dawn and dusk. To determine the relationships among genes responsive to different light quality and light intensity treatments in K. fedtschenkoi, we performed a weighted gene co-expression network analysis (WGCNA) using the DEGs identified from the previous comparisons (Fig. 2). The greatest starch content observed for any filteredlight treatment was seen in dusk samples grown under RL, these starch levels were still much lower than in plants grown under full-spectrum light (Fig. 6d) These low starch accumulation patterns were likely due to the lower photon flux densities delivered to the plants under these light-filtering conditions. Numerous circadian rhythm– related regulators were co-expressed with ABI2, which included CCA1 (Kaladp0496s0018), CCR1 (Kaladp0018s0148), CCR2 (Kaladp0020s0114), COL4 (Kaladp0029s0144), 3 copies of COR27 (Kaladp0011s1228, Kaladp0042s0067, and Kaladp0089s0010), DBB3 (Kaladp0192s0026), 2 copies of ELF4 (Kaladp0037s0163 and Kaladp0045s0206), KT4 (Kaladp0040s0740), LHY1 (Kaladp0066s0115), PRR7 (Kaladp0005s0054), RVE1 (Kaladp0574s0015), RVE2 (Kaladp0262s0019), and RVE7 (Kaladp0262s0013)

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