The CYCLIN-A CYCA1;2/TAM Is Required for the Meiosis I to Meiosis II Transition and Cooperates with OSD1 for the Prophase to First Meiotic Division Transition

Abstract

Meiosis halves the chromosome number because its two divisions follow a single round of DNA replication. This process involves two cell transitions, the transition from prophase to the first meiotic division (meiosis I) and the unique meiosis I to meiosis II transition. We show here that the A-type cyclin CYCA1;2/TAM plays a major role in both transitions in Arabidopsis. A series of tam mutants failed to enter meiosis II and thus produced diploid spores and functional diploid gametes. These diploid gametes had a recombined genotype produced through the single meiosis I division. In addition, by combining the tam-2 mutation with AtSpo11-1 and Atrec8, we obtained plants producing diploid gametes through a mitotic-like division that were genetically identical to their parents. Thus tam alleles displayed phenotypes very similar to that of the previously described osd1 mutant. Combining tam and osd1 mutations leads to a failure in the prophase to meiosis I transition during male meiosis and to the production of tetraploid spores and gametes. This suggests that TAM and OSD1 are involved in the control of both meiotic transitions.

Meiotic Progression inArabidopsisIs Governed by Complex Regulatory Interactions between SMG7, TDM1, and the Meiosis I–Specific Cyclin TAM

“…In an attempt to rescue the smg7 and tdm1 phenotypes, we sought to inactivate a meiotic cyclin and downregulate meiotic CDK. TAM (cyclin A1;2) appeared to be the obvious candidate, as its function is important for meiotic entry as well as for progression into the second meiosis (Wang et al, 2004b(Wang et al, , 2010d'Erfurth et al, 2010; this study). However, we found that neither the hypomorphic tam-1 nor the null tam-2 alleles alleviate the anaphase II arrest in smg7 mutants or the reentry into the third meiosis in tdm1 plants.…”

“…The role of TAM appears to be more complex. TAM is important for entry into the first and second meiotic divisions (Wang et al, 2004b(Wang et al, , 2010d'Erfurth et al, 2010), but its expression seems to be restricted to meiosis I. We suggest that TAM promotes the activities of the core CDK complexes that drive entry into the second meiosis by antagonizing the inhibitory effects of SMG7 and TDM1 ( Figure 8A).…”

Use of 2n Gametes in Plant Breeding

“…A similar male-specific dyad-triad phenotype was observed and characterised in another mutant called jason (De Storme & Geelen, 2011;Erilova et al, 2009). Mutants of two other genes, OSD and TAM (CYCA1;2), were shown to omit the second meiotic division in both male and female sporogenesis at high frequency resulting in the formation of both 2n pollen and egg cells (d'Erfurth et al, 2009(d'Erfurth et al, , 2010.…”

Perturbation of cell cycle regulation triggers plant immune response via activation of disease resistance genes

“…OSD1 and UVI4 are negative regulators of APC/C, which is responsible for degrading cell cycle proteins (12,16). The loss of OSD1 or UVI4 function leads to various defects in cell cycle progression, including omission of meiosis divisions, increased endoreduplication, and possibly increased endomitosis (10)(11)(12)(13)16) Surprisingly, overexpression of either OSD1 or UVI4 leads to spontaneous cell death and enhanced disease resistance to a virulent bacterial pathogen (Fig. 2B).…”

“…OSD1 functions in both divisions of meiosis, and loss of its function leads to omission of the second meiotic division by itself, as well as omission of the first meiotic division hen combined with cycA1;2 (10,11). OSD1 is also involved in endoreduplication or endomitosis in cotyledons, and the loss-of-function (LoF) mutatation osd1 or gig1 (gigas cell 1) has gigantic cotyledon epidermal cells with higher ploidy (12).…”