Transgene containment by maternal inheritance: Effective or elusive?

Abstract

Transgene containment is a central concern in genetically modified (GM) crops, especially for those with out-crossing wild relatives. However, plant cells contain genomes in the nucleus, mitochondria, and chloroplasts. Whereas nuclear genes are biparentally inherited, organelle genes are in general maternally inherited (1, 2). Therefore, engineering foreign genes in the chloroplast genome may provide containment from pollen transmission. This topic was hotly debated when the first herbicide-resistant (Round-Up-ready) transplastomic plants (transformed with chloroplast genomes) were reported (3). In this issue of PNAS, two articles highlight different aspects of this important question. The article by Svab and Maliga (4) examines whether alien cytoplasm contributes to rare paternal plastid transmission. They report low frequencies (10−4 to 10−5) of paternal plastids in both normal and alien cytoplasm and caution that this observation is biased by tissue culture selection, and therefore transgenes are less likely to get into the germ line under field conditions. Most importantly, these investigators show that the entire plastid genome is transmitted by pollen instead of plastid DNA fragments and that the mitochondria are also cotransmitted. In a parallel study, Ruf et al. (5) set up a stringent selection system for paternal transmission by using male-sterile maternal parents and transplastomic pollen donors, conferring plastid-specific antibiotic resistance and green fluorescence for visual screening. This selection system identified 6 among 2.1 million seedlings screened (frequency of 2.86 × 10−6) that showed paternal transmission of transgenes, and the authors concluded that plastid transformation provides an effective tool to increase biosafety of GM crops. Most flowering plants show uniparental maternal inheritance of plastids (2). This observation was first reported a century ago in Milabilis jalapa and is achieved through a variety of mechanisms (2). During pollen development, at the microspore mitosis, all plastids are distributed into vegetative cells, and, therefore, …