Abstract
Brassica rapa RNE participates in the processing of polycistronic precursor transcripts into mature monocistronic mRNAs in plastids, thereby sending strong retrograde signals. Leaf color is one of the most important agronomic traits for Chinese cabbage. Not only is it closely linked to photosynthesis, thereby affecting plant growth, but it also influences consumer preference in the marketplace. A pale-green mutant rne was produced by EMS mutagenesis of Chinese cabbage inbred line A03. Chlorophyll content, photosynthetic rate, actual quantum efficiency (φPSII), and maximum quantum efficiency (Fv/Fm) of photosystem II (PSII) were all reduced in rne plants. Genetic analysis indicated that the pale-green trait was controlled by a pair of recessive alleles. Using mixed pool sequencing of F2 individuals derived from an rne × wild-type cross, we identified the essential gene Brassica rapa RNase E (BrRNE), which is responsible for chloroplast development. BrRNE cleaves polycistronic RNA in Chinese cabbage A03 plastids, but rne plants are defective in RNA processing and show reduced translation levels of the seven plastid genes, BrpsaB, BrpsaA, BrpsbA, BrpsbD, BrpsbB, BrpetA, and Brycf4. Abnormal RNA processing in the plastids sends retrograde signals that markedly regulate the expression of nuclear genes, upregulating genes that participate in ribosome and DNA replication pathways and repressing photosynthesis-associated nuclear genes (PhANGs). Our study reveals a new regulatory mechanism by which plastid RNA cleavage influences plastid development and leaf color, sending retrograde signals that affect the expression of nuclear genes in Brassica.
Highlights
Photosynthesis is essential for plant growth and development, and chlorophyll (Chl) is the main pigment that absorbs light energy and drives electron transport in the photosynthetic reaction centers of higher plants (Tanaka and Tanaka 2006)
Photosynthetic rate was significantly reduced in rne plants (Fig. 1f), as were the actual quantum efficiency and the maximum quantum efficiency of photosystem II (PSII; Fv/Fm), which are standard measures of PSII integrity (Fig. 1g–h)
The top six Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways enriched in downregulated genes were photosynthesis, starch and sucrose metabolism, phorosynthesis-antenna proteins, glyoxylate and dicarboxylate metabolism, plant-pathogen interaction, and carbon fixation in photosynthetic organisms (Fig. 4d). These results suggest that the expression of photosynthesis-associated nuclear genes (PhANGs) is repressed in the rne mutant and that PhANGs with reduced expression in rne primarily functioned in PSI and PSII, light harvesting, carbon fixation, and electron carrier processes (Table S4)
Summary
Photosynthesis is essential for plant growth and development, and chlorophyll (Chl) is the main pigment that absorbs light energy and drives electron transport in the photosynthetic reaction centers of higher plants (Tanaka and Tanaka 2006). Defects in Chl biosynthesis, degradation, or other related pathways often result in leaf color mutants. These mutants are widely distributed in nature and produce a variety of phenotypes, including albino, virescent, chlorina, xanthas, maculate, striped, and dark green (Jung et al 2003; Manjaya 2009; Singh and Ikehashi 1981). Leaf color mutants are ideal genetic materials with which to study the molecular mechanisms of plant photosynthesis and chloroplast development. Previous studies have reported that the main molecular mechanisms of chl-related mutations are: (1) mutations in genes of the chl biosynthesis pathway
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