Featured Publications

Pre-meiotic 21-nucleotide reproductive phasiRNAs emerged in seed plants and diversified in flowering plants

Pokhrel, S, Huang, K, Bélanger, S, Zhan, J, Caplan, JL, Kramer, EM et al.
Nat Commun. 2021;12 (1):4941. doi: 10.1038/s41467-021-25128-y 

Abstract
Plant small RNAs are important regulatory elements that fine-tune gene expression and maintain genome integrity by silencing transposons. Reproductive organs of monocots produce abundant phased, small interfering RNAs (phasiRNAs). The 21-nt reproductive phasiRNAs triggered by miR2118 are highly enriched in pre-meiotic anthers, and have been found in multiple eudicot species, in contrast with prior reports of monocot specificity. The 24-nt reproductive phasiRNAs are triggered by miR2275, and are highly enriched during meiosis in many angiosperms. Here, we report the widespread presence of the 21-nt reproductive phasiRNA pathway in eudicots including canonical and non-canonical microRNA (miRNA) triggers of this pathway. In eudicots, these 21-nt phasiRNAs are enriched in pre-meiotic stages, a spatiotemporal distribution consistent with that of monocots and suggesting a role in anther development. Although this pathway is apparently absent in well-studied eudicot families including the Brassicaceae, Solanaceae and Fabaceae, our work in eudicots supports an earlier singular finding in spruce, a gymnosperm, indicating that the pathway of 21-nt reproductive phasiRNAs emerged in seed plants and was lost in some lineages.

Transgenerational conditioned male fertility of HD-ZIP IV transcription factor mutant ocl4: impact on 21-nt phasiRNA accumulation in pre-meiotic maize anthers

Yadava, P, Tamim, S, Zhang, H, Teng, C, Zhou, X, Meyers, BC et al.
Plant Reprod. 2021;34 (2):117-129. doi: 10.1007/s00497-021-00406-3

Abstract
Environment-sensitive male-sterile plants have been described before and can result from different molecular mechanisms and biological processes, but putative environment-conditioned, transgenerational rescue of their male fertility is a rather new mystery. Here, we report a derivative line of the male-sterile outer cell layer 4 (ocl4) mutant of maize, in which fertility was restored and perpetuated over several generations. Conditioned fertile ocl4 anthers exhibit the anatomical abnormality of a partially duplicated endothecial layer, just like their sterile counterparts. We profiled the dynamics of phased, small interfering RNAs (phasiRNAs) during pre-meiotic development in fully sterile and various grades of semi-fertile ocl4 anthers. The conditioned fertile anthers accumulated significantly higher 21-nt phasiRNAs compared to ocl4 sterile samples, suggesting a partial restoration of phasiRNAs in conditioned fertility. We found that the biogenesis of 21-nt phasiRNAs is largely dependent on Ocl4 at three key steps: (1) production of PHAS precursor transcripts, (2) expression of miR2118 that modulates precursor processing, and (3) accumulation of 21-nt phasiRNAs.

Space: the final frontier - achieving single-cell, spatially resolved transcriptomics in plants

Gurazada, SGR, Cox, KL, Czymmek, KJ, Meyers, BC
Emerg Top Life Sci. 2021;5 (2):179-188. doi: 10.1042/ETLS20200274 

Abstract
Single-cell RNA-seq is a tool that generates a high resolution of transcriptional data that can be used to understand regulatory networks in biological systems. In plants, several methods have been established for transcriptional analysis in tissue sections, cell types, and/or single cells. These methods typically require cell sorting, transgenic plants, protoplasting, or other damaging or laborious processes. Additionally, the majority of these technologies lose most or all spatial resolution during implementation. Those that offer a high spatial resolution for RNA lack breadth in the number of transcripts characterized. Here, we briefly review the evolution of spatial transcriptomics methods and we highlight recent advances and current challenges in sequencing, imaging, and computational aspects toward achieving 3D spatial transcriptomics of plant tissues with a resolution approaching single cells. We also provide a perspective on the potential opportunities to advance this novel methodology in plants.

Reproductive phasiRNA loci and DICER-LIKE5, but not microRNA loci, diversified in monocotyledonous plants

Patel, P, Mathioni, SM, Hammond, R, Harkess, AE, Kakrana, A, Arikit, S et al.
Plant Physiol. 2021;185 (4):1764-1782. doi: 10.1093/plphys/kiab001 

Abstract
In monocots other than maize (Zea mays) and rice (Oryza sativa), the repertoire and diversity of microRNAs (miRNAs) and the populations of phased, secondary, small interfering RNAs (phasiRNAs) are poorly characterized. To remedy this, we sequenced small RNAs (sRNA) from vegetative and dissected inflorescence tissue in 28 phylogenetically diverse monocots and from several early-diverging angiosperm lineages, as well as publicly available data from 10 additional monocot species. We annotated miRNAs, small interfering RNAs (siRNAs) and phasiRNAs across the monocot phylogeny, identifying miRNAs apparently lost or gained in the grasses relative to other monocot families, as well as a number of transfer RNA fragments misannotated as miRNAs. Using our miRNA database cleaned of these misannotations, we identified conservation at the 8th, 9th, 19th, and 3′-end positions that we hypothesize are signatures of selection for processing, targeting, or Argonaute sorting. We show that 21-nucleotide (nt) reproductive phasiRNAs are far more numerous in grass genomes than other monocots. Based on sequenced monocot genomes and transcriptomes, DICER-LIKE5, important to 24-nt phasiRNA biogenesis, likely originated via gene duplication before the diversification of the grasses. This curated database of phylogenetically diverse monocot miRNAs, siRNAs, and phasiRNAs represents a large collection of data that should facilitate continued exploration of sRNA diversification in flowering plants.

100 Most Recent Publications

Huang, K, Demirci, F, Meyers, BC, Caplan, JL. A Novel Method to Map Small RNAs with High Resolution. Bio Protoc. 2021;11 (16):e4128. doi: 10.21769/BioProtoc.4128. PubMed PMID:34541046 PubMed Central PMC8413618.

Wang, L, Zhu, T, Rodriguez, JC, Deal, KR, Dubcovsky, J, McGuire, PE et al.. Aegilops tauschii genome assembly Aet v5.0 features greater sequence contiguity and improved annotation. G3 (Bethesda). 2021; :. doi: 10.1093/g3journal/jkab325. PubMed PMID:34515796 .

Pokhrel, S, Huang, K, Bélanger, S, Zhan, J, Caplan, JL, Kramer, EM et al.. Pre-meiotic 21-nucleotide reproductive phasiRNAs emerged in seed plants and diversified in flowering plants. Nat Commun. 2021;12 (1):4941. doi: 10.1038/s41467-021-25128-y. PubMed PMID:34400639 PubMed Central PMC8368212.

Eckardt, NA, Meyers, BC. The Plant Cell is accepting applications for Assistant Features Editors. Plant Cell. 2021;33 (9):2901. doi: 10.1093/plcell/koab185. PubMed PMID:34312677 .

Pokhrel, S, Huang, K, Meyers, BC. Conserved and non-conserved triggers of 24-nucleotide reproductive phasiRNAs in eudicots. Plant J. 2021;107 (5):1332-1345. doi: 10.1111/tpj.15382. PubMed PMID:34160111 .

Beric, A, Mabry, ME, Harkess, AE, Brose, J, Schranz, ME, Conant, GC et al.. Comparative phylogenetics of repetitive elements in a diverse order of flowering plants (Brassicales). G3 (Bethesda). 2021; :. doi: 10.1093/g3journal/jkab140. PubMed PMID:33993297 .

Chatterjee, D, Wittmeyer, K, Lee, TF, Cui, J, Yennawar, NH, Yennawar, HP et al.. Maize unstable factor for orange1 is essential for endosperm development and carbohydrate accumulation. Plant Physiol. 2021; :. doi: 10.1093/plphys/kiab183. PubMed PMID:33905500 PubMed Central PMC8331166.

Veley, KM, Okwuonu, I, Jensen, G, Yoder, M, Taylor, NJ, Meyers, BC et al.. Gene tagging via CRISPR-mediated homology-directed repair in cassava. G3 (Bethesda). 2021;11 (4):. doi: 10.1093/g3journal/jkab028. PubMed PMID:33855431 PubMed Central PMC8049417.

Eckardt, NA, Meyers, BC. THE PLANT CELL Welcomes New Assistant Features Editors. Plant Cell. 2020;32 (3):527-528. doi: 10.1105/tpc.20.00035. PubMed PMID:33814868 PubMed Central PMC7054029.

Eckardt, NA, Meyers, BC. Sowing the Seeds of Equity and Diversity in Academia and STEM Disciplines. Plant Cell. 2020;32 (11):3371. doi: 10.1105/tpc.20.00692. PubMed PMID:33814867 PubMed Central PMC7610288.

Patel, P, Mathioni, SM, Hammond, R, Harkess, AE, Kakrana, A, Arikit, S et al.. Reproductive phasiRNA loci and DICER-LIKE5, but not microRNA loci, diversified in monocotyledonous plants. Plant Physiol. 2021;185 (4):1764-1782. doi: 10.1093/plphys/kiab001. PubMed PMID:33793935 PubMed Central PMC8133688.

Eckardt, NA, Meyers, BC. Thank You, Editors and Reviewers of The Plant Cell. Plant Cell. 2020;32 (12):3639-3645. doi: 10.1105/tpc.20.00878. PubMed PMID:33792696 PubMed Central PMC7721326.

Blatt, MR, Meyers, BC. ASPB welcomes Oxford University Press. Plant Cell. 2021;33 (1):1. doi: 10.1093/plcell/koaa004. PubMed PMID:33751097 PubMed Central PMC8136877.

Eckardt, NA, Meyers, BC. The Plant Cell welcomes 2021 Assistant Features Editors. Plant Cell. 2021;33 (1):2. doi: 10.1093/plcell/koaa005. PubMed PMID:33751091 PubMed Central PMC8136908.

Yadava, P, Tamim, S, Zhang, H, Teng, C, Zhou, X, Meyers, BC et al.. Transgenerational conditioned male fertility of HD-ZIP IV transcription factor mutant ocl4: impact on 21-nt phasiRNA accumulation in pre-meiotic maize anthers. Plant Reprod. 2021;34 (2):117-129. doi: 10.1007/s00497-021-00406-3. PubMed PMID:33689028 .

Chen, C, Li, J, Feng, J, Liu, B, Feng, L, Yu, X et al.. sRNAanno-a database repository of uniformly annotated small RNAs in plants. Hortic Res. 2021;8 (1):45. doi: 10.1038/s41438-021-00480-8. PubMed PMID:33642576 PubMed Central PMC7917102.

Blatt, MR, Meyers, BC. ASPB welcomes Oxford University Press. Plant Physiol. 2021;185 (1):15. doi: 10.1093/plphys/kiaa025. PubMed PMID:33631816 PubMed Central PMC8133678.

Eckardt, NA, Birchler, JA, Brady, SM, Buell, CR, Leebens-Mack, JH, Meyers, BC et al.. Focus on the biology of plant genomes. Plant Cell. 2021;33 (4):781-782. doi: 10.1093/plcell/koab039. PubMed PMID:33576423 PubMed Central PMC8227447.

Yu, Y, Ji, L, Le, BH, Zhai, J, Chen, J, Luscher, E et al.. Correction: ARGONAUTE10 promotes the degradation of miR165/6 through the SDN1 and SDN2 exonucleases in Arabidopsis. PLoS Biol. 2021;19 (2):e3001120. doi: 10.1371/journal.pbio.3001120. PubMed PMID:33571183 PubMed Central PMC7877630.

Gurazada, SGR, Cox, KL, Czymmek, KJ, Meyers, BC. Space: the final frontier - achieving single-cell, spatially resolved transcriptomics in plants. Emerg Top Life Sci. 2021;5 (2):179-188. doi: 10.1042/ETLS20200274. PubMed PMID:33522561 .

Harkess, A, McLoughlin, F, Bilkey, N, Elliott, K, Emenecker, R, Mattoon, E et al.. Improved Spirodela polyrhiza genome and proteomic analyses reveal a conserved chromosomal structure with high abundance of chloroplastic proteins favoring energy production. J Exp Bot. 2021;72 (7):2491-2500. doi: 10.1093/jxb/erab006. PubMed PMID:33454741 .

Lee, YS, Maple, R, Dürr, J, Dawson, A, Tamim, S, Del Genio, C et al.. A transposon surveillance mechanism that safeguards plant male fertility during stress. Nat Plants. 2021;7 (1):34-41. doi: 10.1038/s41477-020-00818-5. PubMed PMID:33398155 .

Escobar-Tovar, L, Sierra, J, Hernández-Muñoz, A, McQuinn, RP, Mathioni, S, Cordoba, E et al.. Deconvoluting apocarotenoid-mediated retrograde signaling networks regulating plastid translation and leaf development. Plant J. 2021;105 (6):1582-1599. doi: 10.1111/tpj.15134. PubMed PMID:33340183 .

Zhang, M, Ma, X, Wang, C, Li, Q, Meyers, BC, Springer, NM et al.. CHH DNA methylation increases at 24-PHAS loci depend on 24-nt phased small interfering RNAs in maize meiotic anthers. New Phytol. 2021;229 (5):2984-2997. doi: 10.1111/nph.17060. PubMed PMID:33135165 .

Tian, P, Zhang, X, Xia, R, Liu, Y, Wang, M, Li, B et al.. Evolution and diversification of reproductive phased small interfering RNAs in Oryza species. New Phytol. 2021;229 (5):2970-2983. doi: 10.1111/nph.17035. PubMed PMID:33111313 .

Jia, J, Ji, R, Li, Z, Yu, Y, Nakano, M, Long, Y et al.. Soybean DICER-LIKE2 Regulates Seed Coat Color via Production of Primary 22-Nucleotide Small Interfering RNAs from Long Inverted Repeats. Plant Cell. 2020;32 (12):3662-3673. doi: 10.1105/tpc.20.00562. PubMed PMID:33077493 PubMed Central PMC7721327.

Jiang, N, Gutierrez-Diaz, A, Mukundi, E, Lee, YS, Meyers, BC, Otegui, MS et al.. Author Correction: Synergy between the anthocyanin and RDR6/SGS3/DCL4 siRNA pathways expose hidden features of Arabidopsis carbon metabolism. Nat Commun. 2020;11 (1):5276. doi: 10.1038/s41467-020-19223-9. PubMed PMID:33057182 PubMed Central PMC7560853.

Bélanger, S, Pokhrel, S, Czymmek, K, Meyers, BC. Premeiotic, 24-Nucleotide Reproductive PhasiRNAs Are Abundant in Anthers of Wheat and Barley But Not Rice and Maize. Plant Physiol. 2020;184 (3):1407-1423. doi: 10.1104/pp.20.00816. PubMed PMID:32917771 PubMed Central PMC7608162.

Ding, B, Xia, R, Lin, Q, Gurung, V, Sagawa, JM, Stanley, LE et al.. Developmental Genetics of Corolla Tube Formation: Role of the tasiRNA-ARF Pathway and a Conceptual Model. Plant Cell. 2020;32 (11):3452-3468. doi: 10.1105/tpc.18.00471. PubMed PMID:32917737 PubMed Central PMC7610285.

Liu, Y, Teng, C, Xia, R, Meyers, BC. PhasiRNAs in Plants: Their Biogenesis, Genic Sources, and Roles in Stress Responses, Development, and Reproduction. Plant Cell. 2020;32 (10):3059-3080. doi: 10.1105/tpc.20.00335. PubMed PMID:32817252 PubMed Central PMC7534485.

Huang, K, Demirci, F, Batish, M, Treible, W, Meyers, BC, Caplan, JL et al.. Quantitative, super-resolution localization of small RNAs with sRNA-PAINT. Nucleic Acids Res. 2020;48 (16):e96. doi: 10.1093/nar/gkaa623. PubMed PMID:32716042 PubMed Central PMC7498346.

Huang, K, Batish, M, Teng, C, Harkess, A, Meyers, BC, Caplan, JL et al.. Quantitative Fluorescence In Situ Hybridization Detection of Plant mRNAs with Single-Molecule Resolution. Methods Mol Biol. 2020;2166 :23-33. doi: 10.1007/978-1-0716-0712-1_2. PubMed PMID:32710401 .

Grover, JW, Burgess, D, Kendall, T, Baten, A, Pokhrel, S, King, GJ et al.. Abundant expression of maternal siRNAs is a conserved feature of seed development. Proc Natl Acad Sci U S A. 2020;117 (26):15305-15315. doi: 10.1073/pnas.2001332117. PubMed PMID:32541052 PubMed Central PMC7334491.

Teng, C, Zhang, H, Hammond, R, Huang, K, Meyers, BC, Walbot, V et al.. Dicer-like 5 deficiency confers temperature-sensitive male sterility in maize. Nat Commun. 2020;11 (1):2912. doi: 10.1038/s41467-020-16634-6. PubMed PMID:32518237 PubMed Central PMC7283321.

Jiang, N, Gutierrez-Diaz, A, Mukundi, E, Lee, YS, Meyers, BC, Otegui, MS et al.. Synergy between the anthocyanin and RDR6/SGS3/DCL4 siRNA pathways expose hidden features of Arabidopsis carbon metabolism. Nat Commun. 2020;11 (1):2456. doi: 10.1038/s41467-020-16289-3. PubMed PMID:32415123 PubMed Central PMC7229025.

Harkess, A, Huang, K, van der Hulst, R, Tissen, B, Caplan, JL, Koppula, A et al.. Sex Determination by Two Y-Linked Genes in Garden Asparagus. Plant Cell. 2020;32 (6):1790-1796. doi: 10.1105/tpc.19.00859. PubMed PMID:32220850 PubMed Central PMC7268802.

Hossain, MS, Hoang, NT, Yan, Z, Tóth, K, Meyers, BC, Stacey, G et al.. Corrigendum: Characterization of the Spatial and Temporal Expression of Two Soybean miRNAs Identifies SCL6 as a Novel Regulator of Soybean Nodulation. Front Plant Sci. ;10 :1692. doi: 10.3389/fpls.2019.01692. PubMed PMID:32117326 PubMed Central PMC7029589.

Debladis, E, Lee, TF, Huang, YJ, Lu, JH, Mathioni, SM, Carpentier, MC et al.. Construction and characterization of a knock-down RNA interference line of OsNRPD1 in rice (Oryza sativa ssp japonica cv Nipponbare). Philos Trans R Soc Lond B Biol Sci. 2020;375 (1795):20190338. doi: 10.1098/rstb.2019.0338. PubMed PMID:32075556 PubMed Central PMC7061988.

Meyers, BC. New at the Helm of The Plant Cell, a Journal for the Plant Science Community[OPEN]. Plant Cell. 2020;32 (1):1-3. doi: 10.1105/tpc.19.00900. PubMed PMID:33792701 PubMed Central PMC6961624.

Feng, L, Zhang, F, Zhang, H, Zhao, Y, Meyers, BC, Zhai, J et al.. An Online Database for Exploring Over 2,000 Arabidopsis Small RNA Libraries. Plant Physiol. 2020;182 (2):685-691. doi: 10.1104/pp.19.00959. PubMed PMID:31843802 PubMed Central PMC6997705.

Bi, H, Fei, Q, Li, R, Liu, B, Xia, R, Char, SN et al.. Disruption of miRNA sequences by TALENs and CRISPR/Cas9 induces varied lengths of miRNA production. Plant Biotechnol J. 2020;18 (7):1526-1536. doi: 10.1111/pbi.13315. PubMed PMID:31821678 PubMed Central PMC7292542.

Eckardt, NA, Meyers, BC, Merchant, SS. The Plant Cell Is Accepting Applications for Assistant Features Editors. Plant Cell. 2019;31 (11):2545. doi: 10.1105/tpc.19.00787. PubMed PMID:33831150 PubMed Central PMC6881125.

Nakano, M, McCormick, K, Demirci, C, Demirci, F, Gurazada, SGR, Ramachandruni, D et al.. Next-Generation Sequence Databases: RNA and Genomic Informatics Resources for Plants. Plant Physiol. 2020;182 (1):136-146. doi: 10.1104/pp.19.00957. PubMed PMID:31690707 PubMed Central PMC6945852.

Juárez-González, VT, López-Ruiz, BA, Baldrich, P, Luján-Soto, E, Meyers, BC, Dinkova, TD et al.. The explant developmental stage profoundly impacts small RNA-mediated regulation at the dedifferentiation step of maize somatic embryogenesis. Sci Rep. 2019;9 (1):14511. doi: 10.1038/s41598-019-50962-y. PubMed PMID:31601893 PubMed Central PMC6786999.

Crisp, PA, Hammond, R, Zhou, P, Vaillancourt, B, Lipzen, A, Daum, C et al.. Variation and Inheritance of Small RNAs in Maize Inbreds and F1 Hybrids. Plant Physiol. 2020;182 (1):318-331. doi: 10.1104/pp.19.00817. PubMed PMID:31575624 PubMed Central PMC6945832.

Hunt, M, Banerjee, S, Surana, P, Liu, M, Fuerst, G, Mathioni, S et al.. Correction to: small RNA discovery in the interaction between barley and the powdery mildew pathogen. BMC Genomics. 2019;20 (1):697. doi: 10.1186/s12864-019-6012-7. PubMed PMID:31484492 PubMed Central PMC6727339.

Baldrich, P, Meyers, BC. Bacteria send messages to colonize plant roots. Science. 2019;365 (6456):868-869. doi: 10.1126/science.aay7101. PubMed PMID:31467211 .

Ji, L, Mathioni, SM, Johnson, S, Tucker, D, Bewick, AJ, Do Kim, K et al.. Genome-Wide Reinforcement of DNA Methylation Occurs during Somatic Embryogenesis in Soybean. Plant Cell. 2019;31 (10):2315-2331. doi: 10.1105/tpc.19.00255. PubMed PMID:31439802 PubMed Central PMC6790092.

Hunt, M, Banerjee, S, Surana, P, Liu, M, Fuerst, G, Mathioni, S et al.. Small RNA discovery in the interaction between barley and the powdery mildew pathogen. BMC Genomics. 2019;20 (1):610. doi: 10.1186/s12864-019-5947-z. PubMed PMID:31345162 PubMed Central PMC6657096.

Trolet, A, Baldrich, P, Criqui, MC, Dubois, M, Clavel, M, Meyers, BC et al.. Cell Cycle-Dependent Regulation and Function of ARGONAUTE1 in Plants. Plant Cell. 2019;31 (8):1734-1750. doi: 10.1105/tpc.19.00069. PubMed PMID:31189739 PubMed Central PMC6713298.

Hossain, MS, Hoang, NT, Yan, Z, Tóth, K, Meyers, BC, Stacey, G et al.. Characterization of the Spatial and Temporal Expression of Two Soybean miRNAs Identifies SCL6 as a Novel Regulator of Soybean Nodulation. Front Plant Sci. 2019;10 :475. doi: 10.3389/fpls.2019.00475. PubMed PMID:31057581 PubMed Central PMC6477095.

Meyers, BC, Axtell, MJ. MicroRNAs in Plants: Key Findings from the Early Years. Plant Cell. 2019;31 (6):1206-1207. doi: 10.1105/tpc.19.00310. PubMed PMID:31036598 PubMed Central PMC6588298.

Fourounjian, P, Tang, J, Tanyolac, B, Feng, Y, Gelfand, B, Kakrana, A et al.. Post-transcriptional adaptation of the aquatic plant Spirodela polyrhiza under stress and hormonal stimuli. Plant J. 2019;98 (6):1120-1133. doi: 10.1111/tpj.14294. PubMed PMID:30801806 .

Xia, R, Chen, C, Pokhrel, S, Ma, W, Huang, K, Patel, P et al.. 24-nt reproductive phasiRNAs are broadly present in angiosperms. Nat Commun. 2019;10 (1):627. doi: 10.1038/s41467-019-08543-0. PubMed PMID:30733503 PubMed Central PMC6367383.

Baldrich, P, Rutter, BD, Karimi, HZ, Podicheti, R, Meyers, BC, Innes, RW et al.. Plant Extracellular Vesicles Contain Diverse Small RNA Species and Are Enriched in 10- to 17-Nucleotide "Tiny" RNAs. Plant Cell. 2019;31 (2):315-324. doi: 10.1105/tpc.18.00872. PubMed PMID:30705133 PubMed Central PMC6447009.

Huang, K, Baldrich, P, Meyers, BC, Caplan, JL. sRNA-FISH: versatile fluorescent in situ detection of small RNAs in plants. Plant J. 2019;98 (2):359-369. doi: 10.1111/tpj.14210. PubMed PMID:30577085 PubMed Central PMC6465150.

Wittmeyer, K, Cui, J, Chatterjee, D, Lee, TF, Tan, Q, Xue, W et al.. The Dominant and Poorly Penetrant Phenotypes of Maize Unstable factor for orange1 Are Caused by DNA Methylation Changes at a Linked Transposon. Plant Cell. 2018;30 (12):3006-3023. doi: 10.1105/tpc.18.00546. PubMed PMID:30563848 PubMed Central PMC6354275.

Moro, B, Chorostecki, U, Arikit, S, Suarez, IP, Höbartner, C, Rasia, RM et al.. Efficiency and precision of microRNA biogenesis modes in plants. Nucleic Acids Res. 2018;46 (20):10709-10723. doi: 10.1093/nar/gky853. PubMed PMID:30289546 PubMed Central PMC6237749.

Raman, V, Meyers, BC, Dean, RA, Donofrio, NM. Characterizing Small RNAs in Filamentous Fungi Using the Rice Blast Fungus, Magnaporthe oryzae, as an Example. Methods Mol Biol. 2018;1848 :53-66. doi: 10.1007/978-1-4939-8724-5_5. PubMed PMID:30182228 .

Patel, P, Mathioni, S, Kakrana, A, Shatkay, H, Meyers, BC. Reproductive phasiRNAs in grasses are compositionally distinct from other classes of small RNAs. New Phytol. 2018;220 (3):851-864. doi: 10.1111/nph.15349. PubMed PMID:30020552 .

Fei, Q, Yu, Y, Liu, L, Zhang, Y, Baldrich, P, Dai, Q et al.. Biogenesis of a 22-nt microRNA in Phaseoleae species by precursor-programmed uridylation. Proc Natl Acad Sci U S A. 2018;115 (31):8037-8042. doi: 10.1073/pnas.1807403115. PubMed PMID:30012624 PubMed Central PMC6077734.

Richard, MMS, Gratias, A, Meyers, BC, Geffroy, V. Molecular mechanisms that limit the costs of NLR-mediated resistance in plants. Mol Plant Pathol. 2018;19 (11):2516-2523. doi: 10.1111/mpp.12723. PubMed PMID:30011120 PubMed Central PMC6638094.

Kakrana, A, Mathioni, SM, Huang, K, Hammond, R, Vandivier, L, Patel, P et al.. Plant 24-nt reproductive phasiRNAs from intramolecular duplex mRNAs in diverse monocots. Genome Res. 2018;28 (9):1333-1344. doi: 10.1101/gr.228163.117. PubMed PMID:30002159 PubMed Central PMC6120631.

Tamim, S, Cai, Z, Mathioni, SM, Zhai, J, Teng, C, Zhang, Q et al.. Cis-directed cleavage and nonstoichiometric abundances of 21-nucleotide reproductive phased small interfering RNAs in grasses. New Phytol. 2018;220 (3):865-877. doi: 10.1111/nph.15181. PubMed PMID:29708601 .

He, J, Xu, M, Willmann, MR, McCormick, K, Hu, T, Yang, L et al.. Threshold-dependent repression of SPL gene expression by miR156/miR157 controls vegetative phase change in Arabidopsis thaliana. PLoS Genet. 2018;14 (4):e1007337. doi: 10.1371/journal.pgen.1007337. PubMed PMID:29672610 PubMed Central PMC5929574.

Edger, PP, Hall, JC, Harkess, A, Tang, M, Coombs, J, Mohammadin, S et al.. Brassicales phylogeny inferred from 72 plastid genes: A reanalysis of the phylogenetic localization of two paleopolyploid events and origin of novel chemical defenses. Am J Bot. 2018;105 (3):463-469. doi: 10.1002/ajb2.1040. PubMed PMID:29574686 .

Liu, H, Soyars, CL, Li, J, Fei, Q, He, G, Peterson, BA et al.. CRISPR/Cas9-mediated resistance to cauliflower mosaic virus. Plant Direct. 2018;2 (3):e00047. doi: 10.1002/pld3.47. PubMed PMID:31245713 PubMed Central PMC6508564.

van der Linde, K, Timofejeva, L, Egger, RL, Ilau, B, Hammond, R, Teng, C et al.. Pathogen Trojan Horse Delivers Bioactive Host Protein to Alter Maize Anther Cell Behavior in Situ. Plant Cell. 2018;30 (3):528-542. doi: 10.1105/tpc.17.00238. PubMed PMID:29449414 PubMed Central PMC5894838.

Baldrich, P, Beric, A, Meyers, BC. Despacito: the slow evolutionary changes in plant microRNAs. Curr Opin Plant Biol. 2018;42 :16-22. doi: 10.1016/j.pbi.2018.01.007. PubMed PMID:29448158 .

Axtell, MJ, Meyers, BC. Revisiting Criteria for Plant MicroRNA Annotation in the Era of Big Data. Plant Cell. 2018;30 (2):272-284. doi: 10.1105/tpc.17.00851. PubMed PMID:29343505 PubMed Central PMC5868703.

Ma, W, Chen, C, Liu, Y, Zeng, M, Meyers, BC, Li, J et al.. Coupling of microRNA-directed phased small interfering RNA generation from long noncoding genes with alternative splicing and alternative polyadenylation in small RNA-mediated gene silencing. New Phytol. 2018;217 (4):1535-1550. doi: 10.1111/nph.14934. PubMed PMID:29218722 .

Friesner, J, Assmann, SM, Bastow, R, Bailey-Serres, J, Beynon, J, Brendel, V et al.. The Next Generation of Training for Arabidopsis Researchers: Bioinformatics and Quantitative Biology. Plant Physiol. 2017;175 (4):1499-1509. doi: 10.1104/pp.17.01490. PubMed PMID:29208732 PubMed Central PMC5717721.

Wang, PH, Wittmeyer, KT, Lee, TF, Meyers, BC, Chopra, S. Overlapping RdDM and non-RdDM mechanisms work together to maintain somatic repression of a paramutagenic epiallele of maize pericarp color1. PLoS One. 2017;12 (11):e0187157. doi: 10.1371/journal.pone.0187157. PubMed PMID:29112965 PubMed Central PMC5675401.

Harkess, A, Zhou, J, Xu, C, Bowers, JE, Van der Hulst, R, Ayyampalayam, S et al.. The asparagus genome sheds light on the origin and evolution of a young Y chromosome. Nat Commun. 2017;8 (1):1279. doi: 10.1038/s41467-017-01064-8. PubMed PMID:29093472 PubMed Central PMC5665984.

Sidorenko, LV, Lee, TF, Woosley, A, Moskal, WA, Bevan, SA, Merlo, PAO et al.. GC-rich coding sequences reduce transposon-like, small RNA-mediated transgene silencing. Nat Plants. 2017;3 (11):875-884. doi: 10.1038/s41477-017-0040-6. PubMed PMID:29085072 .

Wai, CM, VanBuren, R, Zhang, J, Huang, L, Miao, W, Edger, PP et al.. Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple. Plant J. 2017;92 (1):19-30. doi: 10.1111/tpj.13630. PubMed PMID:28670834 .

Huang, K, Doyle, F, Wurz, ZE, Tenenbaum, SA, Hammond, RK, Caplan, JL et al.. FASTmiR: an RNA-based sensor for in vitro quantification and live-cell localization of small RNAs. Nucleic Acids Res. 2017;45 (14):e130. doi: 10.1093/nar/gkx504. PubMed PMID:28586459 PubMed Central PMC5737440.

Raman, V, Simon, SA, Demirci, F, Nakano, M, Meyers, BC, Donofrio, NM et al.. Small RNA Functions Are Required for Growth and Development of Magnaporthe oryzae. Mol Plant Microbe Interact. 2017;30 (7):517-530. doi: 10.1094/MPMI-11-16-0236-R. PubMed PMID:28504560 .

Xia, R, Xu, J, Meyers, BC. The Emergence, Evolution, and Diversification of the miR390-TAS3-ARF Pathway in Land Plants. Plant Cell. 2017;29 (6):1232-1247. doi: 10.1105/tpc.17.00185. PubMed PMID:28442597 PubMed Central PMC5502456.

Reyes-Chin-Wo, S, Wang, Z, Yang, X, Kozik, A, Arikit, S, Song, C et al.. Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce. Nat Commun. 2017;8 :14953. doi: 10.1038/ncomms14953. PubMed PMID:28401891 PubMed Central PMC5394340.

Mathioni, SM, Kakrana, A, Meyers, BC. Characterization of Plant Small RNAs by Next Generation Sequencing. Curr Protoc Plant Biol. 2017;2 (1):39-63. doi: 10.1002/cppb.20043. PubMed PMID:31725976 .

Yu, Y, Ji, L, Le, BH, Zhai, J, Chen, J, Luscher, E et al.. ARGONAUTE10 promotes the degradation of miR165/6 through the SDN1 and SDN2 exonucleases in Arabidopsis. PLoS Biol. 2017;15 (2):e2001272. doi: 10.1371/journal.pbio.2001272. PubMed PMID:28231321 PubMed Central PMC5322904.

Fan, Y, Yang, J, Mathioni, SM, Yu, J, Shen, J, Yang, X et al.. PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proc Natl Acad Sci U S A. 2016;113 (52):15144-15149. doi: 10.1073/pnas.1619159114. PubMed PMID:27965387 PubMed Central PMC5206514.

Nan, GL, Zhai, J, Arikit, S, Morrow, D, Fernandes, J, Mai, L et al.. MS23, a master basic helix-loop-helix factor, regulates the specification and development of the tapetum in maize. Development. 2017;144 (1):163-172. doi: 10.1242/dev.140673. PubMed PMID:27913638 .

Fei, Q, Yang, L, Liang, W, Zhang, D, Meyers, BC. Dynamic changes of small RNAs in rice spikelet development reveal specialized reproductive phasiRNA pathways. J Exp Bot. 2016;67 (21):6037-6049. doi: 10.1093/jxb/erw361. PubMed PMID:27702997 PubMed Central PMC5100018.

Paim Pinto, DL, Brancadoro, L, Dal Santo, S, De Lorenzis, G, Pezzotti, M, Meyers, BC et al.. The Influence of Genotype and Environment on Small RNA Profiles in Grapevine Berry. Front Plant Sci. 2016;7 :1459. doi: 10.3389/fpls.2016.01459. PubMed PMID:27761135 PubMed Central PMC5050227.

Zhang, Y, Xia, R, Kuang, H, Meyers, BC. The Diversification of Plant NBS-LRR Defense Genes Directs the Evolution of MicroRNAs That Target Them. Mol Biol Evol. 2016;33 (10):2692-705. doi: 10.1093/molbev/msw154. PubMed PMID:27512116 PubMed Central PMC5026261.

Char, SN, Neelakandan, AK, Nahampun, H, Frame, B, Main, M, Spalding, MH et al.. An Agrobacterium-delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize. Plant Biotechnol J. 2017;15 (2):257-268. doi: 10.1111/pbi.12611. PubMed PMID:27510362 PubMed Central PMC5259581.

Yang, L, Qian, X, Chen, M, Fei, Q, Meyers, BC, Liang, W et al.. Regulatory Role of a Receptor-Like Kinase in Specifying Anther Cell Identity. Plant Physiol. 2016;171 (3):2085-100. doi: 10.1104/pp.16.00016. PubMed PMID:27208278 PubMed Central PMC4936546.

Wendel, JF, Jackson, SA, Meyers, BC, Wing, RA. Evolution of plant genome architecture. Genome Biol. 2016;17 :37. doi: 10.1186/s13059-016-0908-1. PubMed PMID:26926526 PubMed Central PMC4772531.

Fei, Q, Zhang, Y, Xia, R, Meyers, BC. Small RNAs Add Zing to the Zig-Zag-Zig Model of Plant Defenses. Mol Plant Microbe Interact. 2016;29 (3):165-9. doi: 10.1094/MPMI-09-15-0212-FI. PubMed PMID:26867095 .

Khatabi, B, Arikit, S, Xia, R, Winter, S, Oumar, D, Mongomake, K et al.. High-resolution identification and abundance profiling of cassava (Manihot esculenta Crantz) microRNAs. BMC Genomics. 2016;17 :85. doi: 10.1186/s12864-016-2391-1. PubMed PMID:26822616 PubMed Central PMC4730657.

Curtin, SJ, Michno, JM, Campbell, BW, Gil-Humanes, J, Mathioni, SM, Hammond, R et al.. MicroRNA Maturation and MicroRNA Target Gene Expression Regulation Are Severely Disrupted in Soybean dicer-like1 Double Mutants. G3 (Bethesda). 2015;6 (2):423-33. doi: 10.1534/g3.115.022137. PubMed PMID:26681515 PubMed Central PMC4751560.

Patel, P, Ramachandruni, SD, Kakrana, A, Nakano, M, Meyers, BC. miTRATA: a web-based tool for microRNA Truncation and Tailing Analysis. Bioinformatics. 2016;32 (3):450-2. doi: 10.1093/bioinformatics/btv583. PubMed PMID:26454275 .

Zhai, J, Bischof, S, Wang, H, Feng, S, Lee, TF, Teng, C et al.. A One Precursor One siRNA Model for Pol IV-Dependent siRNA Biogenesis. Cell. 2015;163 (2):445-55. doi: 10.1016/j.cell.2015.09.032. PubMed PMID:26451488 PubMed Central PMC5023148.

Cao, X, Meyers, BC. Editorial overview: Cell signalling and gene regulation-communication and control as the twin pillars of systems biology. Curr Opin Plant Biol. 2015;27 :v-viii. doi: 10.1016/j.pbi.2015.09.001. PubMed PMID:26433830 .

Xia, R, Xu, J, Arikit, S, Meyers, BC. Extensive Families of miRNAs and PHAS Loci in Norway Spruce Demonstrate the Origins of Complex phasiRNA Networks in Seed Plants. Mol Biol Evol. 2015;32 (11):2905-18. doi: 10.1093/molbev/msv164. PubMed PMID:26318183 PubMed Central PMC4651229.

Zhang, H, Xia, R, Meyers, BC, Walbot, V. Evolution, functions, and mysteries of plant ARGONAUTE proteins. Curr Opin Plant Biol. 2015;27 :84-90. doi: 10.1016/j.pbi.2015.06.011. PubMed PMID:26190741 .

Xia, R, Ye, S, Liu, Z, Meyers, BC, Liu, Z. Novel and Recently Evolved MicroRNA Clusters Regulate Expansive F-BOX Gene Networks through Phased Small Interfering RNAs in Wild Diploid Strawberry. Plant Physiol. 2015;169 (1):594-610. doi: 10.1104/pp.15.00253. PubMed PMID:26143249 PubMed Central PMC4577376.

Fei, Q, Li, P, Teng, C, Meyers, BC. Secondary siRNAs from Medicago NB-LRRs modulated via miRNA-target interactions and their abundances. Plant J. 2015;83 (3):451-65. doi: 10.1111/tpj.12900. PubMed PMID:26042408 .

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