Loss-of-Function Mutants and Overexpression Lines of the Arabidopsis Cyclin CYCA1;2/TARDY ASYNCHRONOUS MEIOSIS Exhibit Different Defects in Prophase-I Meiocytes but Produce the Same Meiotic Products

Abstract

In Arabidopsis, loss-of-function mutations in the A-type cyclin CYCA1;2/TARDY ASYNCHRONOUS MEIOSIS (TAM) gene lead to the production of abnormal meiotic products including triads and dyads. Here we report that overexpression of TAM by the ASK1:TAM transgene also led to the production of triads and dyads in meiosis, as well as shriveled seeds, in a dominant fashion. However, the partial loss-of-function mutant tam-1, an ASK1:TAM line, and the wild type differed in dynamic changes in chromosome thread thickness from zygotene to diplotene. We also found that the pericentromeric heterochromatin regions in male meiocytes in tam-1 and tam-2 (a null allele) frequently formed a tight cluster at the pachytene and diplotene stages, in contrast to the infrequent occurrences of such clusters in the wild type and the ASK1:TAM line. Immunolocalization studies of the chromosome axial component ASY1 revealed that ASY1 was highly expressed at the appropriate male meiotic stages but not localized to the chromosomes in tam-2. The level of ASY1, however, was greatly reduced in another ASK1:TAM line with much overexpressed TAM. Our results indicate that the reduction and increase in the activity of TAM differentially affect chromosomal morphology and the action of ASY1 in prophase I. Based on these results, we propose that either the different meiotic defects or a common defect such as missing ASY1 on the chromosomal axes triggers a hitherto uncharacterized cell cycle checkpoint in the male meiocytes in the tam mutants and ASK1:TAM lines, leading to the production of the same abnormal meiotic products.

Spatiotemporal features of microsporogenesis in the cycad species Macrozamia communis

“…(F) Microsporocytes likely at the pachytene stage; starch grains were no longer at one pole of the cell, and evenly thick chromosomes threads had appeared. These prophase‐I stages were deciphered largely based on well‐documented prophase‐I features of Arabidopsis male meiosis (Wang and Yang, 2014). (G, H) Fluorescence images of semithin sections.…”

Complex haploinsufficient interaction between APC11 and CYCLIN A1;2/TARDY ASYNCHRONOUS MEIOSIS in embryo development and seed germination in Arabidopsis

“…No mutants of these cyclins have been shown to produce an embryo-defective or a seedgermination-defective phenotype, even though gene expression studies have implicated a role in embryo development and/or seed germination for most of them, including TARDY ASYNCHRONOUS MEIOSIS (TAM)/CYCA1;2 (Masubelele et al 2005;Narsai et al 2011;Hofmann et al 2019). Homozygous tam-1/tam-1 and tam-2/tam-2 mutants are defective in meiotic cell cycle progression and in nuclear size regulation in trichomes and guard cells, but no obvious defect was observed in their embryo development and seed germination (Magnard et al 2001;Wang et al 2004;Wang et al 2010;Jha et al 2014;Wang and Yang 2014). The previous studies also did not reveal any defect in heterozygous TAM/tam-1 and TAM/tam-2 plants.…”

The plant‐specific protein FEHLSTART controls male meiotic entry, initializing meiotic synchronization in Arabidopsis

“…Furthermore, mutations in TAM lead to a failure to enter meiosis II, and thus to the production of diploid but functional gametes, indicating a role in the meiosis I/II transition (d'Erfurth et al ., ). A recent study comparing loss‐of‐function mutants and overexpression lines of TAM detected diverse defects in prophase I meiocytes that converged in the same meiotic products, including dyads and triads, supporting a TAM function during progression of meiosis (Wang and Yang, ).…”

“…In Arabidopsis the synchrony of male meiosis seems to be established during meiotic interphase (Ito and Takegami, ; Hamant et al ., ). A class of cyclin or cyclin‐dependent kinase proteins is believed to be essential for the maintenance of meiotic synchrony, for example Arabidopsis TARDY ASYNCHRONOUS MEIOSIS (TAM; also known as CYCA1;2) (Wang et al ., ; Wang and Yang, ). Meiosis in tam mutants is asynchronous and delayed.…”