Multi-omics analysis reveals regulation of rhizome swelling in Nelumbo nucifera

Abstract The swelling of crop storage organs is an important agronomic trait with high economic value. However, the signals influencing storage organ swelling are not fully understood. Here, we assembled a high-quality genome of the rhizome-type Asian lotus (Nelumbo nucifera Gaertn.), comprising 759 Mb with 99.98% of sequences anchored to 8 chromosomes. Comparative genome analyses revealed conserved synteny with the China Antique Asian lotus and identified 64,886 structural variants. We observed physiological changes during development of the lotus rhizome from the major stolon to the swelling phase. The swelling transition stage was identified as a critical period for initiation of rhizome swelling. Global DNA methylation increased during the rhizome swelling process, mainly due to increased CHH methylation; this correlated with decreased expression of DNA demethylase genes. Large-scale time-series analysis of transcriptome dynamics revealed that differentially methylated genes and differentially expressed genes associated with plant hormone signal transduction and the metabolic processes of sucrose and starch are closely related to rhizome swelling. We analyzed expression patterns and co-expressed modules specific to the stolon to swelling stages and found the auxin pathway to be particularly active during the transition stage. Auxin response factor (ARF) transcription factors were identified as core regulators of the network during the transition stage. Furthermore, the experiments showed that auxin elicits interactions between NnARF2 and Sucrose Transporter1/2 (NnSUT1/2), Starch Synthase1 (NnSS1), and NnARF12 interacts with Starch Branching Enzyme II (NnSBEII) to directly activate source–sink synergy-mediated starch accumulation and increase yield. In conclusion, our findings provide insight into the effects of DNA methylation and auxin on swelling and source–sink sucrose transport regulation.