title: Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers.
abstract: Maize anthers, the male reproductive floral organs, express two classes of phased small-interfering RNAs (phasiRNAs). PhasiRNA precursors are transcribed by RNA polymerase II and map to low-copy, intergenic regions similar to PIWI-interacting RNAs (piRNAs) in mammalian testis. From 10 sequential cohorts of staged maize anthers plus mature pollen we find that 21-nt phased siRNAs from 463 loci appear abruptly after germinal and initial somatic cell fate specification and then diminish, whereas 24-nt phasiRNAs from 176 loci coordinately accumulate during meiosis and persist as anther somatic cells mature and haploid gametophytes differentiate into pollen. Male-sterile ocl4 anthers defective in epidermal signaling lack 21-nt phasiRNAs. Male-sterile mutants with subepidermal defects--mac1 (excess meiocytes), ms23 (defective pretapetal cells), and msca1 (no normal soma or meiocytes)--lack 24-nt phasiRNAs. ameiotic1 mutants (normal soma, no meiosis) accumulate both 21-nt and 24-nt phasiRNAs, ruling out meiotic cells as a source or regulator of phasiRNA biogenesis. By in situ hybridization, miR2118 triggers of 21-nt phasiRNA biogenesis localize to epidermis; however, 21-PHAS precursors and 21-nt phasiRNAs are abundant subepidermally. The miR2275 trigger, 24-PHAS precursors, and 24-nt phasiRNAs all accumulate preferentially in tapetum and meiocytes. Therefore, each phasiRNA type exhibits independent spatiotemporal regulation with 21-nt premeiotic phasiRNAs dependent on epidermal and 24-nt meiotic phasiRNAs dependent on tapetal cell differentiation. Maize phasiRNAs and mammalian piRNAs illustrate putative convergent evolution of small RNAs in male reproduction.
authors.affiliation: Department of Plant and Soil Sciences and Delaware Biotechnology Institute, University of Delaware, Newark, DE 19716; and.
authors.forename: Jixian
authors.initials: J
authors.lastname: Zhai
authors.affiliation: Department of Biology, Stanford University, Stanford, CA 94305.
authors.forename: Han
authors.initials: H
authors.lastname: Zhang
authors.affiliation: Department of Plant and Soil Sciences and Delaware Biotechnology Institute, University of Delaware, Newark, DE 19716; and.
authors.forename: Siwaret
authors.initials: S
authors.lastname: Arikit
authors.affiliation: Department of Plant and Soil Sciences and Delaware Biotechnology Institute, University of Delaware, Newark, DE 19716; and.
authors.forename: Kun
authors.initials: K
authors.lastname: Huang
authors.affiliation: Department of Biology, Stanford University, Stanford, CA 94305.
authors.forename: Guo-Ling
authors.initials: GL
authors.lastname: Nan
authors.affiliation: Department of Biology, Stanford University, Stanford, CA 94305 meyers@dbi.udel.edu walbot@stanford.edu.
authors.forename: Virginia
authors.initials: V
authors.lastname: Walbot
authors.affiliation: Department of Plant and Soil Sciences and Delaware Biotechnology Institute, University of Delaware, Newark, DE 19716; and meyers@dbi.udel.edu walbot@stanford.edu.
authors.forename: Blake C
authors.initials: BC
authors.lastname: Meyers
mesh_terms: D008540:Meiosis / Q000235:genetics*; D018749:RNA, Plant / Q000235:genetics*; D003313:Zea mays / Q000166:cytology / Q000502:physiology*
chemical_list: D018749:RNA, Plant
keywords: anther development; phasiRNAs; piRNAs; tapetum; tasiRNAs