Whole-genome de novo assemblies reveal extensive structural variations and dynamic organelle-to-nucleus DNA transfers in African and Asian rice

Abstract

Asian cultivated rice (Oryza sativa) and African cultivated rice (Oryza glaberrima) originated from the wild rice species Oryza rufipogon and Oryza barthii, respectively. The genomes of both cultivated species have undergone profound changes during domestication. Whole-genome de novo assemblies of O. barthii, O. glaberrima, O. rufipogon and Oryza nivara, produced using PacBio single-molecule real-time (SMRT) and next-generation sequencing (NGS) technologies, showed that Gypsy-like retrotransposons are the major contributors to genome size variation in African and Asian rice. Through the detection of genome-wide structural variations (SVs), we observed that besides 28 shared SV hot spots, another 67 hot spots existed in either the Asian or African rice genomes. Based on gene annotation information of the SVs, we established that organelle-to-nucleus DNA transfers resulted in numerous SVs that participated in the nuclear genome divergence of rice species and subspecies. We detected 52 giant nuclear integrants of organelle DNA (NORGs, defined as >10 kb) in six Oryza AA genomes. In addition, we developed an effective method to genotype giant NORGs, based on genome assembly, and first showed the dynamic change in the distribution of giant NORGs in rice natural population. Interestingly, 16 highly differentiated giant NORGs tended to accumulate in natural populations of Asian rice from higher latitude regions, grown at lower temperatures and light intensities. Our study provides new insight into the genome divergence of African and Asian rice, and establishes that organelle-to-nucleus DNA transfers, as potentially powerful contributors to environmental adaptation during rice evolution, play a major role in producing SVs in rice genomes.

Keywords: African and Asian rice; de novo assembly; organelle-to-nucleus DNA transfer; structural variation.