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Plastome variation, including single spontaneous nucleotide substitutions and single insertions/deletions, is the major source of leaf variegation in plants. Additionally, one recent study has showed that a simple plastome structural variation, which is induced by one pair of small inverted repeats, can also result in leaf variegation. Here we show a complex plastome structural variation caused by intermolecular and intramolecular recombination across three pairs of small inverted repeats accounts for leaf variegation in a widely cultivated shrub Heptapleurum ellipticum (Araliaceae). This plastome structural variation contains two deletions and two duplications, resulting in dramatic expansion of IRs, substantial contraction of LSC and loss of 11 genes that essential for photosynthesis. Plastome heteroplasmy was detected in both green and albino sectors of variegated leaves. Relative to green sectors, albino sectors in the variegated leaves exhibit significantly reduced expression for the 11 genes lost in the mutated plastome as well as 26 other genes, but significantly increased expression for one gene related to translation apparatus. Optical and transmission electron microscopy observations showed that mesophyll cells of albino sectors possess plastids lacking grana lamellae, which likely carry the mutated plastome and contribute to albinism. In both sectors, the first layer of spongy mesophyll cells beneath the lower epidermis contains normal chloroplasts, suggesting periclinal division of the lower epidermis during development. Our study demonstrates that multiple small repeats can collectively mediate intra- and inter-molecular recombination in plastome and offers a new mechanism accounting for leaf variegation in plants. • A complex plastome structural variation caused by small- repeats mediated recombination was identified in Heptapleurum . • This plastome structural variation results in the loss of 11 genes that affect photosynthesis. • Albino sectors in the variegated leaves exhibit significantly reduced expression for the 11 genes. • Mesophyll cells of albino sectors likely carry the mutated plastome. • Our study offers a new mechanism accounting for leaf variegation in plants.
Ma et al. (Tue,) studied this question.