Leaf variegation caused by plastome structural variation: an example from Dianella tasmanica

Abstract

Variegated plants often exhibit plastomic heteroplasmy due to single-nucleotide mutations or small insertions/deletions in their albino sectors. Here, however, we identified a plastome structural variation in albino sectors of the variegated plant Dianella tasmanica (Asphodelaceae), a perennial herbaceous plant widely cultivated as an ornamental in tropical Asia. This structural variation, caused by intermolecular recombination mediated by an 11-bp inverted repeat flanking a 92-bp segment in the large single-copy region (LSC), generates a giant plastome (228 878 bp) with the largest inverted repeat of 105 226 bp and the smallest LSC of 92 bp known in land plants. It also generates an ∼7-kb deletion on the boundary of the LSC, which eliminates three protein coding genes (psbA, matK, and rps16) and one tRNA gene (trnK). Albino sectors exhibit dramatic changes in expression of many plastid genes, including negligible expression of psbA, matK, and rps16, reduced expression of photosynthesis-related genes, and increased expression of genes related to the translational apparatus. Microscopic and ultrastructure observations showed that albino tissues were present in both green and albino sectors of the variegated individuals, and chloroplasts were poorly developed in the mesophyll cells of the albino tissues of the variegated individuals. These poorly developed chloroplasts likely carry the large and rearranged plastome, which is likely responsible for the loss of photosynthesis and albinism in the leaf margins. Considering that short repeats are relatively common in plant plastomes and that photosynthesis is not necessary for albino sectors, structural variation of this kind may not be rare in the plastomes of variegated plants.

Acknowledgements

We thank Shiquan Liang, Sanya Ke, and Qi Zeng for their help with plant sampling. This study was supported financially by the National Natural Science Foundation of China (31811530297).

Author contributions

R.Z. designed the research, S.Z., Y.L., and K.M. performed the research and analyzed the data, and R.Z., S.Z., Y.L., and J.P.M. wrote the paper.

Data availability

Raw Illumina DNA reads of five samples of D. tasmanica have been deposited in the NCBI SRA database (https://www.ncbi.nlm.nih.gov/sra) under accession numbers SRR25393521-SRR25393525. Raw nanopore reads of one sample of D. tasmanica have been deposited in the NCBI SRA database under accession number SRR26974411. Raw Illumina RNA-seq reads of six samples of D. tasmanica have been deposited in the NCBI SRA database under accession numbers SRR25409419-SRR25409423 and SRR25409519. Sequences and annotations of the G-type and A-type plastomes of D. tasmanica are available in NCBI GenBank (https://www.ncbi.nlm.nih.gov/genbank) under accession numbers OR345355 and OR345356.

Conflict of interest

No conflict of interest declared.

Supplementary data

Supplementary data is available at Horticulture Research online.

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