Comparative analyses of American and Asian lotus genomes reveal insights into petal color, carpel thermogenesis and domestication

Abstract

SUMMARY Nelumbo lutea (American lotus), which differs from Nelumbo nucifera (Asian lotus) morphologically, is one of the two remaining species in the basal eudicot family Nelumbonaceae. Here, we assembled the 843‐Mb genome of American lotus into eight pseudochromosomes containing 31 382 protein‐coding genes. Comparative analyses revealed conserved synteny without large chromosomal rearrangements between the genomes of American and Asian lotus and identified 29 533 structural variants (SVs). Carotenoid and anthocyanin pigments determine the yellow and red petal colors of American and Asian lotus, respectively. The structural genes encoding enzymes of the carotenoid and anthocyanin biosynthesis pathways were conserved between two species but differed in expression. We detected SVs caused by repetitive sequence expansion or contraction among the anthocyanin biosynthesis regulatory MYB genes. Further transient overexpression of candidate NnMYB5 induced anthocyanin accumulation in lotus petals. Alternative oxidase (AOX), uncoupling proteins (UCPs), and sugar metabolism and transportation contributed to carpel thermogenesis. Carpels produce heat with sugars transported from leaves as the main substrates, because there was weak tonoplast sugar transporter (TST) activity, and with SWEETs were highly expressed during thermogenesis. Cell proliferation‐related activities were particularly enhanced in the warmer carpels compared with stamens during the cold night before blooming, which suggested that thermogenesis plays an important role in flower protogyny. Population genomic analyses revealed deep divergence between American and Asian lotus, and independent domestication affecting seed, rhizome, and flower traits. Our findings provide a high‐quality reference genome of American lotus for exploring the genetic divergence and variation between two species and revealed possible genomic bases for petal color, carpel thermogenesis and domestication in lotus.

Studies on Lotus Genomics and the Contribution to Its Breeding

“…It is interesting to investigate the dramatic difference in repeat sequence between them because most protein-coding genes show a one-to-one synteny pattern. A total of 29,533 structure variations (SVs) were detected between two lotus species, with the SV-associated genes overexpressed in 'regulation of mitotic cell cycle', and 'protein transporter activity' [25]. Meanwhile, this study also showed that the selection on an MYB gene might contribute to the color difference between Asian and American lotus [25].…”

“…Although it is known that there are only two species of lotus, namely Asian lotus and American lotus, except for the difference in flower color, their plant architecture and morphology are very similar. Based on molecular phylogeny analysis, significant genetic differentiation between American and Asian lotus was verified [25][26][27][28]. De-novo deep sequencing of the American lotus showed that its genome size is 843 Mb, and an approximate 81% repeat sequence was identified (Table 1), which is larger than the genome of Asian lotus.…”

“…3", was also assembled using the Oxford Nanopore sequencing platform (57.9 Gb raw data) with the contig N50 being 5.1 Mb, and eight chromosomes were anchored based on high-throughput chromatin conformation capture (Hi-C) data [24]. Another lotus species, American lotus, was recently assembled using PacBio RSII (74.6 Gb raw data) and Hi-C (50.32 Gb raw data), and the total length is 843 Mb while contig N50 is 1.34 Mb [25]. These data demonstrate that long-read sequencing technology has greatly improved the quality of the lotus genome.…”

“…High-quality genome assembly of "Taikonglian NO. 3" and American lotus genome were also recently generated [24,25]. High-throughput re-sequencing of different lotus cultivars has been utilized to identify numerous molecular markers, promoting marker-assisted selection.…”

Comprehensive Analysis for GRF Transcription Factors in Sacred Lotus (Nelumbo nucifera)

“…and N. lutea Willd. [ 22 ]. N. nucifera is mainly distributed in China, India, Japan, Australia, and Iran [ 23 ].…”