Genome-wide analysis and functional annotation of chromatin-enriched noncoding RNAs in rice during somatic cell regeneration

Abstract

Background Plants have the remarkable ability to generate callus, a pluripotent cell mass that acquires competence for subsequent tissue regeneration. Global chromatin remodeling is required for this cell fate transition, but how the process is regulated is not fully understood. Chromatin-enriched noncoding RNAs (cheRNAs) are thought to play important roles in maintaining chromatin state. However, whether cheRNAs participate in somatic cell regeneration in plants has not yet been clarified. Results To uncover the characteristics and functions of cheRNAs during somatic cell reprogramming in plants, we systematically investigate cheRNAs during callus induction, proliferation and regeneration in rice. We identify 2284 cheRNAs, most of which are novel long non-coding RNAs or small nucleolar RNAs. These cheRNAs, which are highly conserved across plant species, shuttle between chromatin and the nucleoplasm during somatic cell regeneration. They positively regulate the expression of neighboring genes via specific RNA motifs, which may interact with DNA motifs around cheRNA loci. Large-scale mutant analysis shows that cheRNAs are associated with plant size and seed morphology. Further detailed functional investigation of two che-lncRNAs demonstrates that their loss of function impairs cell dedifferentiation and plant regeneration, highlighting the functions of cheRNAs in regulating the expression of neighboring genes via specific motifs. These findings support cis- regulatory roles of cheRNAs in influencing a variety of rice traits. Conclusions cheRNAs are a distinct subclass of regulatory non-coding RNAs that are required for somatic cell regeneration and regulate rice traits. Targeting cheRNAs has great potential for crop trait improvement and breeding in future.

Identification and Functional Analysis of Long Non-Coding RNA (lncRNA) in Response to Seed Aging in Rice

“…In this study, 6002 rice candidate lncRNAs were identified. The number of lncRNAs was about twice as many as lncNATs, and the proportion was similar to the results reported by Zhang [ 63 ]. This group of lncRNAs may be informative for functional genomic studies in rice, especially regarding the mechanisms associated with seed aging.…”

“…LncRNA can regulate target genes in cis- and trans-ways, and the corresponding analysis methods of co-localization and co-expression can be used to predict the function of lncRNAs [ 40 , 41 , 46 , 63 ]. Many studies have been reported based on the cis-regulated target genes of lncRNAs.…”

“…The most well-known lncRNAs in plants, such as COOLAIR and COLDAIR , are closely linked to the expression and regulation of their cis-regulated genes [ 40 , 41 ]. It was found that chromatin-enriched lncRNAs may be local enhancers that affect the expression of multiple genes in rice [ 63 ]. In addition to cis-regulated relationships, trans-regulated networks can be considered in the analysis process.…”

Regulatory non-coding RNAs: Emerging roles during plant cell reprogramming and in vitro regeneration

“…Also, an overrepresentation of 24 nt siRNAs was associated with SE synchronism (Zhang et al, 2014). Thus, as noted by Dal Santo et al, (2022), a readjustment of 24 nt siRNAs appears to be essential for embryogenic commitment.…”

“…Recently, chromatin-enriched ncRNAs (cheRNAs) were identified as positive regulators of genes related to somatic cell reprogramming, being required for cell dedifferentiation and plant regeneration ability in rice ( Zhang et al., 2022 ).…”