Examination of the Cytoplasmic DNA in Male Reproductive Cells to Determine the Potential for Cytoplasmic Inheritance in 295 Angiosperm Species

Abstract

Mature pollen grains of 295 angiosperm species were screened by epifluorescence microscopy for a marker that denotes the mode of cytoplasmic inheritance. We used the DNA fluorochrome DAPI (4',6-diamidino-2-phenylindole) for pollen cell staining. The presence or absence of fluorescence of cytoplasmic DNA in the generative cell or sperm cells was examined in each species. The species examined represented 254 genera and 98 families, and 40 of these families had not been previously studied in this regard. The cytoplasmic DNA of the generative cell or sperm cells did not fluoresce in 81% of the species examined, from 83% of the genera and 87% of the families examined, indicating the potential for maternal cytoplasmic inheritance in these species. In contrast, the male reproductive cells of 19% of the species, from 17% of the genera and 26% of the families examined, displayed fluorescence of the cytoplasmic DNA, indicating the potential for biparental cytoplasmic inheritance in these species. The results revealed the potential for biparental cytoplasmic inheritance in several species in which the inheritance mode was previously unknown, including plants in the Bignoniaceae, Cornaceae, Cruciferae (Brassicaceae), Cyperaceae, Dipsacaceae, Hydrocharitaceae, Papaveraceae, Portulacaceae, Tiliaceae, Valerianaceae, and Zingiberaceae. Electron microscopy revealed that the sperm cells of Portulaca grandiflora contain both plastid and mitochondrial DNA. However, in the generative cells of Musella lasiocarpa, the mitochondria contain DNA, but the plastids do not. These data provide a foundation for further studies of cytoplasmic inheritance in angiosperms.

A Conserved, Mg2+-Dependent Exonuclease Degrades Organelle DNA duringArabidopsisPollen Development

“…Irrespective of the inheritance mode, however, we noticed that organelle DNAs are cytologically absent in pollen vegetative cells (Matsushima et al, 2008a;Sakamoto et al, 2008). A survey of numerous mature pollen grains using DAPI staining has revealed that almost all angiosperm species lack cytologically detectable organelle DNAs in pollen vegetative cells (Corriveau and Coleman, 1988;Mogensen, 1996;Zhang et al, 2003;Wang et al, 2010). It is noteworthy that pollen vegetative cells do not contribute to fertilization, but they do contain numerous plastids and mitochondria, which might be necessary for a pollen tube to germinate, elongate, and deliver sperm cells into the embryo sac.…”

Chloroplast Biogenesis: Control of Plastid Development, Protein Import, Division and Inheritance

“…However, there is an apparent bias in the proportion of their occurrence (Kuroiwa, 1991;Mogensen, 1996;Hagemann, 2004). In angiosperms, maternal inheritance dominates over the others: cytological studies (see below) suggest that approximately 80% of all species show maternal inheritance, and that the remaining species show biparental inheritance (Corriveau and Coleman, 1988;Zhang et al, 2003). In contrast, uniparental paternal inheritance of plastids is very rare, and is only reported in the kiwi plant (Actinidia deliciosa).…”

“…In contrast, such DAPI signals are not detected in maternal inheritance species (Miyamura et al, 1987). This disparity serves as a convenient method for assessing the 'potential' for biparental inheritance (Corriveau and Coleman, 1988;Zhang et al, 2003). In fact, it has enabled us to estimate that 80% of angiosperms exhibit maternal inheritance.…”

Molecular Identification of "Chuanxiong" by Nucleotide Sequence and Multiplex Single Base Extension Analysis on Chloroplast trnK Gene

“…The trnK gene sequence determined in the present study which belongs to chloroplast DNA is mostly of maternal inheritance in angiosperm. 26) Our results suggested that at least C. officinale and L. chuanxiong were not from the same maternal line. Morphology, cytogenetic characters 9,10) and chemical constitutions [10][11][12] revealed the 2 species were quite different.…”