Genome-wide analyses across Viridiplantae reveal the origin and diversification of small RNA pathway-related genes

Abstract

Small RNAs play a major role in the post-transcriptional regulation of gene expression in eukaryotes. Despite the evolutionary importance of streptophyte algae, knowledge on small RNAs in this group of green algae is almost non-existent. We used genome and transcriptome data of 34 algal and plant species, and performed genome-wide analyses of small RNA (miRNA & siRNA) biosynthetic and degradation pathways. The results suggest that Viridiplantae started to evolve plant-like miRNA biogenesis and degradation after the divergence of the Mesostigmatophyceae in the streptophyte algae. We identified two major evolutionary transitions in small RNA metabolism in streptophyte algae; during the first transition, the origin of DCL-New, DCL1, AGO1/5/10 and AGO4/6/9 in the last common ancestor of Klebsormidiophyceae and all other streptophytes could be linked to abiotic stress responses and evolution of multicellularity in streptophytes. During the second transition, the evolution of DCL 2,3,4, and AGO 2,3,7 as well as DRB1 in the last common ancestor of Zygnematophyceae and embryophytes, suggests their possible contribution to pathogen defense and antibacterial immunity. Overall, the origin and diversification of DICER and AGO along with several other small RNA pathway-related genes among streptophyte algae suggested progressive adaptations of streptophyte algae during evolution to a subaerial environment.

A novel class of long small RNAs associates with Argonaute1 and is up-regulated by nutrient deprivation in the alga Chlamydomonas

“…RNA interference, mediated by small noncoding RNAs, is a highly-conserved process influencing gene regulation, genome stability as well as defense responses against genomic parasites (Ghildiyal and Zamore, 2009; Borges and Martienssen, 2015; Wendte and Pikaard, 2017; Yu et al, 2017; Bartel, 2018; Lee and Carroll, 2018; Ozata el al., 2019; Chen and Rechavi, 2021). In multicellular eukaryotes, such as land plants, animals and fungi, extensive duplication and diversification of RNAi machinery components have resulted in complex, partly overlapping pathways for epigenetic regulation (Ghildiyal and Zamore, 2009; Czech and Hannon, 2011; Borges and Martienssen, 2015; Lee and Carroll, 2018; Wang et al, 2021). Duplicated RNAi components appear to allow the evolution of new gene regulatory mechanisms that use distinct sRNAs as sequence-specific determinants, as well as more effective strategies to counteract the action of invading viruses and transposable elements.…”

“…It is generally accepted that sRNA-mediated silencing evolved as a defense mechanism against viruses and transposable elements and was later adapted to regulate the expression of endogenous genes (Cerutti and Casas-Mollano, 2006; Shabalina and Koonin, 2008). Extensive duplication and specialization of proteins involved in sRNA biogenesis and/or effector functions have contributed to pathway diversification (Ghildiyal and Zamore, 2009; Swarts et al, 2014; Borges and Martienssen, 2015; Lee and Carroll, 2018; Wang et al, 2021; Chen and Rechavi, 2021); and the sorting of sRNAs into specific AGOs/effector complexes ultimately determines their biological function(s) (Ghildiyal and Zamore, 2009; Czech and Hannon, 2011; Borges and Martienssen, 2015; Iwakawa and Tomari, 2022). In land plants, the structure of sRNA duplex precursors (such as thermodynamic asymmetry), the presence and location of mismatches and bulges, as well as the identity of the 5’-terminal nucleotide of sRNAs affect their loading onto individual AGOs and the choice of guide strand (Mi et al, 2008; Takeda et al, 2008; Havecker et al, 2010; Czech and Hannon, 2011; Zhu et al, 2011; Frank et al, 2012; Endo et al, 2013; Zhang et al, 2014; Borges and Martienssen, 2015; Iwakawa and Tomari, 2022).…”

Genome-Wide Analysis of the MADS-Box Gene Family in Holoparasitic Plants (Balanophora subcupularis and Balanophora fungosa var. globosa)

“…Reports on the evolutionary mechanism of phenotypic adaptation indicated gene loss can be beneficial by providing an evolutionary mechanism for phenotypic adaptation ( Albalat and Cañestro, 2016 ; Sahu et al, 2019 ; Wang et al, 2021 ; Li et al, 2022 ). Studies on the flowering mechanism of C. australis show that in order to ensure flowering, dodder eavesdropped on the flowering signal of the host and kept the synchronization of flowering ( Sun et al, 2018 ; Shen et al, 2020 ).…”

Comparative phylogeny and evolutionary analysis of Dicer-like protein family in two plant monophyletic lineages

“…sRNA-mediated gene regulation is one of the fundamental molecular mechanisms having a pivotal role in the regulation of their cognate gene(s) expression in a locus-specific manner at both transcriptional level by DNA methylation and posttranscriptional level via mRNA cleavage and, or translational inhibition [ 14 , 40 ]. sRNAs and their processing pathways are conserved and have distributed in almost all eukaryotes [ 15 , 23 , 46 ]. Such regulatory mechanisms are essential for fine-tuning the expression of the corresponding genes [ 25 ].…”