Maize AMEIOTIC1 is essential for multiple early meiotic processes and likely required for the initiation of meiosis

Abstract

Molecular mechanisms that initiate meiosis have been studied in fungi and mammals, but little is known about the mechanisms directing the meiosis transition in other organisms. To elucidate meiosis initiation in plants, we characterized and cloned the ameiotic1 (am1) gene, which affects the transition to meiosis and progression through the early stages of meiotic prophase in maize. We demonstrate that all meiotic processes require am1, including expression of meiosis-specific genes, establishment of the meiotic chromosome structure, meiosis-specific telomere behavior, meiotic recombination, pairing, synapsis, and installation of the meiosis-specific cytoskeleton. As a result, in most am1 mutants premeiotic cells enter mitosis instead of meiosis. Unlike the genes involved in initiating meiosis in yeast and mouse, am1 also has a second downstream function, whereby it regulates the transition through a novel leptotene-zygotene checkpoint, a key step in early meiotic prophase. The am1 gene encodes a plant-specific protein with an unknown biochemical function. The AM1 protein is diffuse in the nucleus during the initiation of meiosis and then binds to chromatin in early meiotic prophase I when it regulates the leptotene-zygotene progression.chromosomes ͉ plant development ͉ genetics ͉ recombination

OsAM1 is required for leptotene-zygotene transition in rice

“…These results indicate that PMCs in Osam1 are halted at the leptotene-zygotene transition. A similar phenomenon of meiotic arrest in maize involving an am1-praI mutant suggests the presence of a novel checkpoint in maize [24], and supports the notion that the leptotene-zygotene transition checkpoint may also exist in rice.…”

“…Four swi1 alleles [20,21,43,44] and six am1 alleles [22][23][24] have been reported. The two proteins, SWI1 and AM1 have similar functions in the early phases of meiosis, such as regulation of chromosome structure and control of homologous recombination.…”

“…In the am1-1 (ameiotic1-1) mutant allele of maize, both male and female meiocytes fail to enter meiosis; instead, they proceed with several mitotic divisions and then degrade. Plants containing the am1-praI (ameiotic1-prophase I arrest) allele enter meiotic prophase and are arrested at the leptotene-zygotene transition [22][23][24]. Both genes appear to be required for early meiotic events, e.g., for SCC and initiation of synapsis.…”

Developmental switches that hold the key to a revolution in crop biotechnology

“…Genetic variation among the progeny could be avoided by eliminating or suppressing meiotic recombination or meiosis itself. Although basic meiotic processes are conserved among species, diverse mechanisms control the mitosis-to-meiosis transition 3 . For example, the genes IME1 and IME2 in budding yeast, mei2 in fission yeast, stimulated by retinoic acid 8 (Stra8) in mice and ameiotic1 (am1) in maize regulate the initiation of meiosis in different ways 3 .…”

“…Although basic meiotic processes are conserved among species, diverse mechanisms control the mitosis-to-meiosis transition 3 . For example, the genes IME1 and IME2 in budding yeast, mei2 in fission yeast, stimulated by retinoic acid 8 (Stra8) in mice and ameiotic1 (am1) in maize regulate the initiation of meiosis in different ways 3 . In A. thaliana, mutants in which female meiosis is abolished -such as dyad (also known as swi1) mutants 4,5 , spo11 rec8 osd1 triple mutants 6 or ago9 mutants that fail to silence a transposable element-derived small RNA pathway 7 produce a functional but unreduced, diploid FG.…”