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Title: Persistence and protection of mitochondrial DNA in the generative cell of cucumber is consistent with its paternal transmission

Author
item SHEN, JIA - Nanjing Agricultural University
item ZHAO, JUAN - Nanjing Agricultural University
item BARTOSZEWSKI, G - Warsaw University Of Life Sciences
item MALEPSZY, STEFAN - Warsaw University Of Life Sciences
item Havey, Michael
item CHEN, JINFENG - Nanjing Agricultural University

Submitted to: Plant and Cell Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/20/2015
Publication Date: 9/26/2015
Publication URL: http://handle.nal.usda.gov/10113/61703
Citation: Shen, J., Zhao, J., Bartoszewski, G., Malepszy, S., Havey, M., Chen, J. 2015. Persistence and protection of mitochondrial DNA in the generative cell of cucumber is consistent with its paternal transmission. Plant And Cell Physiology. 56(11):2271-2282. doi: 10.1093/pcp/pcv140.

Interpretive Summary: Cucumber, unlike most plants, shows paternal inheritance of its mitochondrial DNA (mtDNA); however, the mechanisms regulating this unique transmission mode are unclear. Here we monitored the amounts of mtDNA through the development of cucumber microspores to pollen and observed that mtDNA decreases in the vegetative cell, but persists in the generative cell that ultimately develops into sperm cells. We characterized the cucumber gene (CsDPD1) similar to the Arabidopsis defective in pollen organelle DNA degradation 1 (AtDPD1) gene, which plays the direct role in mtDNA degradation. CsDPD1 rescued the Arabidopsis mutant at DPD1, indicating the same function in both plants. Expression of CsDPD1 coincides with the decrease of mtDNA in pollen, except in the generative cell, where both the expression and mtDNA levels remain high. Our cytological results confirmed that the persistence of mtDNA in cucumber generative cell is consistent with paternal transmission of the mtDNA. Our molecular analyses suggest that protection of mtDNA in the generative cell is critical factor for paternal mtDNA transmission, rather than mtDNA degradation mediated by CsDPD1. Taken together, these findings indicate that a mechanism may protect paternal mtDNA from degradation and likely be the genetic basis of paternal mtDNA transmission. These results will be of interest to plant geneticists interested in understanding organellar transmission and traits.

Technical Abstract: Cucumber, unlike most plants, shows paternal inheritance of its mitochondrial DNA (mtDNA); however, the mechanisms regulating this unique transmission mode are unclear. Here we monitored the amounts of mtDNA through the development of cucumber microspores to pollen and observed that mtDNA decreases in the vegetative cell, but persists in the generative cell that ultimately develops into sperm cells. We characterized the cucumber homolog (CsDPD1) of the Arabidopsis defective in pollen organelle DNA degradation 1 (AtDPD1) gene, which plays the direct role in mtDNA degradation. CsDPD1 rescued the Arabidopsis mutant at DPD1, indicating the same function in both plants. Expression of CsDPD1 coincides with the decrease of mtDNA in pollen, except in the generative cell, where both the expression and mtDNA levels remain high. Our cytological results confirmed that the persistence of mtDNA in cucumber generative cell is consistent with paternal transmission of the mtDNA. Our molecular analyses suggest that protection of mtDNA in the generative cell is critical factor for paternal mtDNA transmission, rather than mtDNA degradation mediated by CsDPD1. Taken together, these findings indicate that a mechanism may protect paternal mtDNA from degradation and likely be the genetic basis of paternal mtDNA transmission.