DCL5

Endoribonuclease Dicer-like 5 (DCL5)
Identifiers
OrganismZea mays
SymbolDCL5
Alt. symbolsZm00001eb045380
Other data
EC numberEC:3.1.26.3

DICER-LIKE 5 (DCL5) is a plant Dicer-like endoribonuclease that functions in the biogenesis of 24-nucleotide reproductive phased small interfering RNAs (phasiRNAs). The gene is specific to monocots and plays a central role during early anther development, where these small RNAs accumulate at high levels.[1]

DCL5 originated through duplication and functional specialization of DCL3, giving rise to a distinct small RNA pathway associated with plant reproduction.[2]

Evolution

Phylogenetic analyses indicate that DCL5 arose early in monocot evolution, likely before the diversification of grasses, and is absent from most eudicots.[3] Comparative genomics further places the origin of DCL5 at or before early-diverging monocots such as Acorus americanus, suggesting an ancient duplication event followed by lineage-specific retention.[4]

This duplication led to functional divergence between DCL3 and DCL5, with DCL3 primarily associated with heterochromatic siRNA pathways and DCL5 specialized for reproductive phasiRNA production in monocots.[5]

The diversification of DCL5 parallels the expansion and diversification of reproductive phasiRNA loci in monocots, indicating co-evolution of this enzyme with its small RNA substrates.[3]

Function

DCL5 processes precursor transcripts into 24-nucleotide reproductive phasiRNAs that accumulate during premeiotic and meiotic stages of anther development.[6] DCL5 specifically mediates the biogenesis of reproductive phasiRNAs, a subclass of phased small interfering RNAs enriched in premeiotic and meiotic anthers.[6]

These small RNAs are derived from PHAS precursor transcripts that are converted into double-stranded RNA and then processed into phased small interfering RNAs by DCL5.[1] In some nongrass monocots, many 24-nt reproductive phasiRNA precursors are predicted to form foldback or intramolecular duplex structures, indicating that DCL5-associated 24-nt reproductive phasiRNA biogenesis can proceed through more than one precursor structure or biogenesis pathway.[7] In the canonical pathway, meiotic 24-nt reproductive phasiRNAs are triggered by the microRNA miR2275, which directs phased processing of precursor transcripts.[8]

Genetic and molecular studies in rice initially identified this monocot-specific Dicer protein (DCL3b, later renamed DCL5) responsible for 24-nt phasiRNA production, distinct from DCL4, which generates 21-nt phasiRNAs.[8]

Unlike DCL3, which processes RNA polymerase IV-derived transcripts, DCL5 acts primarily on transcripts generated by RNA polymerase II, reflecting mechanistic divergence between these pathways.[5]

Role in plant reproduction

DCL5 is essential for normal male reproductive development in grasses. Loss-of-function mutations in DCL5 lead to depletion of 24-nt reproductive phasiRNAs and defects in pollen development.[1] In maize and wheat, dcl5 mutants exhibit temperature-sensitive male sterility, indicating that the DCL5 pathway contributes to fertility under specific environmental conditions.[1][9]

Recent work suggests that some 24-nt reproductive phasiRNA biogenesis can occur independently of microRNA-directed cleavage and instead may involve conserved sequence motifs that guide DCL5-associated processing.[9]

These findings support a model in which DCL5-dependent phasiRNAs contribute to transcriptional regulation and developmental robustness during male gametophyte formation.

See also

References

  1. ^ a b c d Teng, C.; Zhang, H.; Hammond, R.; Huang, K.; Meyers, B. C.; Walbot, V. (2020). "Dicer-like 5 deficiency confers temperature-sensitive male sterility in maize". Nature Communications. 11 (1): 2912. doi:10.1038/s41467-020-16634-6. PMID 32518237.
  2. ^ Margis, R.; Fusaro, A. F.; Smith, N. A.; Curtin, S. J.; Watson, J. M.; Finnegan, E. J.; Waterhouse, P. M. (2006). "The evolution and diversification of Dicers in plants". FEBS Letters. 580 (10): 2442–2450. doi:10.1016/j.febslet.2006.03.072. PMID 16638569.
  3. ^ a b Patel, P.; Mathioni, S. M.; Hammond, R.; Harkess, A. E.; Kakrana, A.; Arikit, S.; Dusia, A.; Meyers, B. C. (2021). "Reproductive phasiRNA loci and DICER-LIKE5, but not microRNA loci, diversified in monocotyledonous plants". Plant Physiology. 185 (4): 1764–1782. doi:10.1093/plphys/kiab001. PMC 8133688. PMID 33793935.{{cite journal}}: CS1 maint: PMC format (link)
  4. ^ Bélanger, S.; Zhan, J.; Meyers, B. C. (2023). "Phylogenetic analyses of seven protein families refine the evolution of small RNA pathways in green plants". Plant Physiology. 192 (2): 1183–1203. doi:10.1093/plphys/kiad141. PMC 10231463. PMID 36869858.{{cite journal}}: CS1 maint: PMC format (link)
  5. ^ a b Chen, S.; Liu, W.; Naganuma, M.; Tomari, Y.; Iwakawa, H.-o. (2022). "Functional specialization of monocot DCL3 and DCL5 proteins through the evolution of the PAZ domain". Nucleic Acids Research. 50 (8): 4669–4684. doi:10.1093/nar/gkac223. PMID 35380679.
  6. ^ a b Zhai, J.; Zhang, H.; Arikit, S.; Huang, K.; Nan, G.; Walbot, V.; Meyers, B. C. (2015). "Spatiotemporally dynamic, cell-type–dependent premeiotic and meiotic phasiRNAs in maize anthers". Proceedings of the National Academy of Sciences USA. 112 (10): 3146–3151. doi:10.1073/pnas.1418918112. PMID 25713378.
  7. ^ Kakrana, A.; Mathioni, S. M.; Huang, K.; Hammond, R.; Vandivier, L.; Patel, P.; Arikit, S.; Shevchenko, O.; Harkess, A. E.; Kingham, B.; Gregory, B. D.; Leebens-Mack, J. H.; Meyers, B. C. (2018). "Plant 24-nt reproductive phasiRNAs from intramolecular duplex mRNAs in diverse monocots". Genome Research. 28 (9): 1333–1344. doi:10.1101/gr.228163.117. PMC 6120631. PMID 30002159.{{cite journal}}: CS1 maint: PMC format (link)
  8. ^ a b Song, X.; Li, P.; Zhai, J.; Zhou, M.; Ma, L.; Liu, B.; Jeong, D.-H.; Nakano, M.; Cao, S.; Liu, C.; Chu, C.; Wang, X.-J.; Green, P. J.; Meyers, B. C.; Cao, X. (2012). "Roles of DCL4 and DCL3b in rice phased small RNA biogenesis". The Plant Journal. 69 (3): 462–474. doi:10.1111/j.1365-313X.2011.04805.x. PMID 21973320.
  9. ^ a b Bélanger, S.; Martín, A. C.; Marchant, D. B.; Zhan, J.; McGregor, M.; Smedley, M.; Hayta, S.; Moore, G.; Meyers, B. C. (2025). "DICER-LIKE 5 loss causes thermosensitive male sterility in durum wheat and reveals an AU-rich motif guiding 24-nt phasiRNA biogenesis". Proceedings of the National Academy of Sciences USA. 122 (31) e2504349122. doi:10.1073/pnas.2504349122. PMC 12337324. PMID 40737328.{{cite journal}}: CS1 maint: PMC format (link)
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