Abstract
The cucurbit organellar DNAs possess distinctive characteristics of practical and theoretical significance. Whereas the cucurbit chloroplast DNAs are similar in size, structure, and transmission to most Angiosperms, their mitochondrial DNAs show enormous size differences. Plants in the genus Cucumis have some of the largest mitochondrial DNAs among all plants, due in part to accumulation of repetitive DNAs and inter-genomic transfers. Recombination among these repetitive motifs produces structurally diverse mitochondrial DNAs associated with paternally transmitted mosaic phenotypes and altered gene expression. The mitochondrial DNAs of Cucumis species are paternally transmitted, which is relatively rare among Angiosperms. The unique characteristics of the Cucumis organelles are interesting not only from an evolutionary point-of-view, but also may allow for characterization of beneficial organellar-nuclear interactions, generation of mitochondrial mutants, transformation of the mitochondrial DNA, and knock-downs of mitochondrial-gene expression.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsLiterature Cited
Abreu I, Santos A, Salema R. Atypical mitochondria during microsporogenesis in Cucumis sativus L. J Submicroscopy Cytology. 1982;14:369–75.
Ali A, Bang SW, Yang EM, Chung SM, Staub JE. Putative paternal factors controlling chilling tolerance in Korean market-type cucumber (Cucumis sativus L.). Sci Hortic. 2014;167:145–8.
Allen JO, Fauron CM, Minx P, Roark L, Oddiraju S, Lin G, et al. Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics. 2007;177:1173–92.
Alverson AJ, Rice DW, Dickinson S, Barry K, Palmer JD. Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell. 2011;23:2499–513.
Alverson AJ, Wei X, Rice DW, Stern DB, Barry K, Palmer JD. Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). Mol Biol Evol. 2010;27:1436–48.
Alwen A, Eller N, Kastler M, Benito Moreno R, Heberle-Bors E. Potential of in vitro pollen maturation for gene transfer. Physiol Plant. 1990;79:194–6.
Atkin OK, Macherel D. The crucial role of plant mitochondria in orchestrating drought tolerance. Ann Bot. 2009;103:581–97.
Bartoszewski G, Havey MJ, Ziółkowska A, Długosz M, Malepszy S. The selection of mosaic (MSC) phenotype after passage of cucumber (Cucumis sativus L.) through cell culture – a method to obtain plant mitochondrial mutants. J Appl Genet. 2007;1:1–9.
Bartoszewski G, Katzir N, Havey MJ. Organization of repetitive DNAs and the genomic regions carrying ribosomal RNA, cob, and atp9 genes in the cucurbit mitochondrial genomes. Theor Appl Genet. 2004a;108:982–92.
Bartoszewski G, Malepszy S, Havey MJ. Mosaic (MSC) cucumbers regenerated from independent cell cultures possess different mitochondrial rearrangements. Curr Genet. 2004b;45:45–53.
Bartoszewski G, Gawronski P, Szklarczyk M, Verbakel H, Havey MJ. A one-megabase physical map of the cucumber mitochondrial DNA reveals low density and occasional clustering of genes. Genome. 2009;52:299–307.
Bendich AJ, Gauriloff LP. Morphometric analysis of cucurbit mitochondria: the relationship between chondriome volume and DNA content. Protoplasma. 1984;119:1–7.
Bentley KE, Mandel JR, McCauley DE. Paternal leakage and heteroplasmy of mitochondrial genomes in Silene vulgaris: evidence from experimental crosses. Genetics. 2010;185:961–8.
Boynton JJ, Harris EH, Burkhart BD, Lamerson PM, Gillham NW. Transmission of mitochondrial and chloroplast genomes of Chlamydomonas. Proc Natl Acad Sci U S A. 1987;84:2391–5.
Butow RA, Henke RM, Moran JV, Selcher SM, Perlman PS. Transformation of Saccharomyces cerevisiae mitochondria using the biolistic gun. Methods Enzymol. 1996;264:265–78.
Cheng L, Li H, Qu B, Huang T, Tu J, Fu T, et al. Chloroplast transformation of rapeseed (Brassica napus) by particle bombardment of cotyledons. Plant Cell Rep. 2010;29:371–81.
Chung SM, Staub JE, Fazio G. Inheritance of chilling injury: a maternally inherited trait in cucumber. J Amer Soc Hort Sci. 2003;128:526–30.
Chung SM, Staub JE, Chen JF. Molecular phylogeny of Cucumis species as revealed by consensus chloroplast SSR marker length and sequence variation. Genome. 2006;49:219–29.
Chung SM, Gordon V, Staub JE. Sequencing cucumber (Cucumis sativus L.) chloroplast genomes identifies differences between chilling-tolerant and -susceptible cucumber lines. Genome. 2007;50:215–25.
Corriveau J, Coleman A. Rapid screening method to detect biparental inheritance of plastid DNA and results from over 200 angiosperm species. Amer J Bot. 1988;75:1443–58.
Del Valle-Echevarria A, Kiełkowska A, Bartoszewski G, Havey MJ. The mosaic (MSC) mutants of cucumber: a method to produce knock-downs of mitochondrial transcripts. Genes Genomes Genetics (G3). 2015;5:2011–21.
Emanuelsson O, Nielsen H, Brunak S, von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol. 2000;300:1005–16.
Erickson L, Kemble R. Paternal inheritance of mitochondria in rapeseed (Brassica napus). Mol Gen Genet. 1990;222:135–9.
Erickson L, Kemble R, Swanson E. The Brassica mitochondrial plasmid can be sexually transmitted. Pollen transfer of a cytoplasmic genetic element. Mol Gen Genet. 1989;218:419–22.
Fauré S, Noyer JL, Carreel F, Horry JP, Bakry F, Lanaud CL. Maternal inheritance of chloroplast genome and paternal inheritance of mitochondrial genome in bananas (Musa acuminata). Curr Genet. 1994;25:265–9.
Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C. Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays. 2006;28:1091–101.
Giegé P, Sweetlove LJ, Cognat V, Leaver CJ. Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell. 2005;17:1497–512.
Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem. 2010;48:909–30.
Gillham NW. Organelle heredity. New York: Raven; 1978.
Gottlieb RA. Mitochondria: execution central. FEBS Lett. 2000;482:6–12.
Handa H. The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res. 2003;31:5907–16.
Harris SA, Ingram R. Chloroplast DNA and biosystematics: the effects of intraspecific diversity and plastid transmission. Taxon. 1991;40:393–412.
Havey MJ, McCreight JD, Rhodes B, Taurick G. Differential transmission of the Cucumis organellar genomes. Theor Appl Genet. 1998;97:122–8.
Havey MJ, Lilly JW, Bohanec B, Bartoszewski G, Malepzy S. Cucumber: a model angiosperm for mitochondrial transformation? J Appl Genet. 2002;43:1–17.
Havey MJ. Predominant paternal transmission of the cucumber mitochondrial genome. J Heredity. 1997;88:232–5.
Hutchins AE, Youngner VB. Maternal inheritance of a color variation (chimera) in the squash, Cucurbita maxima Duch. J Amer Soc Hort Sci. 1952;60:370–8.
Jacobs HT. Making mitochondrial mutants. Trends Genet. 2001;17:653–60.
Juszczuk I, Flexas J, Szal B, Dąbrowska Z, Ribas-Carbo M, Rychter A. Effect of mitochondrial genome rearrangement on respiratory activity, photosynthesis, photorespiration and energy status of MSC16 cucumber mutant. Physiol Plant. 2007;131:527–41.
Kihira H. Importance of cytoplasm in plant genetics. Cytologia. 1982;47:435–50.
Kim J, Jung J, Lee J, Park H, Oh K, Jeong W, et al. Complete sequence and organization of the cucumber (Cucumis sativus L. cv. Baekmibaekdadagi) chloroplast genome. Plant Cell Rep. 2006;25:334–40.
Kindle KL, Richards KL, Stern DB. Engineering the chloroplast genome: techniques and capabilities for chloroplast transformation of Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A. 1991;88:1721–5.
Kocyan A, Zhang LB, Schaefer H, Renner SS. A multi-locus phylogeny for the Cucurbitaceae and its implications for character evolution and classification. Mol Phylogen Evol. 2007;44:553–77.
Ładyżyński M, Burza W, Malepszy S. Relationship between somaclonal variation and type of culture in cucumber. Euphytica. 2002;125:349–56.
Lilly JW, Havey MJ. Small, repetitive DNAs contribute significantly to the expanded mitochondrial genome of cucumber. Genetics. 2001;159:317–28.
Lilly JW, Bartoszewski G, Malepszy S, Havey MJ. A major deletion in the cucumber mitochondrial genome sorts with the MSC phenotype. Curr Genet. 2001;40:144–51.
Lim H, Gounaris I, Hardison RC, Boyer CD. Restriction site and genetic map of Cucurbita pepo chloroplast DNA. Curr Genet. 1990;18:273–5.
Mackenzie S, McIntosh L. Higher plant mitochondria. Plant Cell. 1999;11:571–85.
Malepszy S, Burza W, Śmiech M. Characterization of a cucumber (Cucumis sativus L.) somaclonal variant with paternal inheritance. J Appl Genet. 1996;37:65–78.
Mason R, Holsinger K, Jansen R. Biparental inheritance of the chloroplast genome in Coreopsis (Asteraceae). J Heredity. 1994;85:171–3.
Matsuura S. Paternal inheritance of mitochondrial DNA in cucumber (Cucumis sativus L.). Report Cucurbit Genet Coop. 1995;18:31–3.
McCauley DE, Bailey MF, Sherman NA, Darnell MZ. Evidence for paternal transmission and heteroplasmy in the mitochondrial genome of Silene vulgaris, a gynodioecious plant. Heredity. 2005;95:50–8.
Medgyesy P, Pay A, Marton L. Transmission of paternal chloroplasts in Nicotiana. Mol Gen Genet. 1986;204:195–8.
Millar AH, Mittova V, Kiddle G, Heazlewood JL, Bartoli CG, Theodoulou FL, et al. Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol. 2003;133:443–7.
Neale DB, Sederoff R. Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theor Appl Genet. 1989;77:212–6.
Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, et al. The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics. 2002;268:434–45.
Ogihara Y, Yamazaki Y, Murai K, Kanno A, Terachi T, Shiina T, et al. Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome. Nucleic Acids Res. 2005;33:6235–50.
Palmer J. Physical and gene mapping of chloroplast DNA from Atriplex triangularis and Cucumis sativus. Nucleic Acids Res. 1982;10:1593–605.
Pearl SA, Welch ME, McCauley DE. Mitochondrial heteroplasmy and paternal leakage in natural populations of Silene vulgaris, a gynodioecious plant. Mol Biol Evol. 2009;26:537–45.
Perl-Treves R, Galun E. The Cucumis plastome: physical map, intrageneric variation, and phylogenetic relationships. Theor Appl Genet. 1985;71:417–29.
Pląder W, Yukawa Y, Sugiura M, Malepszy S. The complete structure of the cucumber (Cucumis sativus L.) chloroplast genome: its composition and comparative analysis. Cell Mol Biol Lett. 2007;12:587–94.
Randolph-Anderson BL, Boynton JE, Gillham NW, Harris EH, Johnson AM, Dorthu MP, et al. Further characterization of the respiratory deficient dum-1 mutation of Chlamydomonas reinhardtii and its use as a recipient for mitochondrial transformation. Mol Gen Genet. 1993;238:235–44.
Ray DT, McCreight JD. Yellow-tip: a cytoplasmically inherited trait in melon (Cucumis melo L.). J Heredity. 1996;87:245–7.
Reape T, McCabe P. Apoptotic-like programmed cell death in plants. New Phytol. 2008;180:13–26.
Rodríguez-Moreno L, González V, Benjak A, Martí M, Puigdomènech P, Aranda M, et al. Determination of the melon chloroplast and mitochondrial genome sequences reveals that the largest reported mitochondrial genome in plants contains a significant amount of DNA having a nuclear origin. BMC Genomics. 2011;12:424.
Ruf S, Hermann M, Berger IJ, Carrer H, Bock R. Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nat Biotechnol. 2001;19:870–5.
Schaefer H, Heibl C, Renner SS. Gourds afloat: a dated phylogeny reveals an Asian origin of the gourd family (Cucurbitaceae) and numerous oversea dispersal events. Proc Royal Soc B. 2009;276:843–51.
Sebastian P, Schaefer H, Telford I, Renner SS. Cucumber (Cucumis sativus) and melon (C. melo) have numerous wild relatives in Asia and Australia, and the sister species of melon is from Australia. Proc Natl Acad Sci U S A. 2010;107:14269–73.
Shen J, Kere MG, Chen JF. Mitochondrial genome is paternally inherited in Cucumis allotetraploid (C. × hytivus) derived by interspecific hybridization. Sci Hortic. 2013;155:39–42.
Shen J, Zhao J, Bartoszewski G, Malepszy S, Havey MJ, Chen JF. Persistence and protection of mitochondrial DNA in the generative cell of cucumber is consistent with its paternal transmission. Plant Cell Physiol. 2015a;56:2271–82.
Shen J, Dirks R, Havey MJ. Diallel crossing among doubled haploids of cucumber reveals significant reciprocal-cross differences. J Amer Soc Hort Sci. 2015b;140:178–82.
Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, Palmer JD, et al. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 2012;10:e1001241.
Smith SE. Influence of paternal genotype on plastid inheritance in Medicago sativa. J Heredity. 1989;80:214–7.
Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, et al. The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Genet Genomics. 2005;272:603–15.
Svab Z, Maliga P. High frequency plastid transformation by selection for a chimeric aadA gene. Proc Natl Acad Sci U S A. 1993;90:913–7.
Szal B, Łukawska K, Zdolińska I, Rychter AM. Chilling stress and mitochondrial genome rearrangement in the MSC16 cucumber mutant affect the alternative oxidase and antioxidant defense system to a similar extent. Physiol Plant. 2009;137:435–45.
Unseld M, Marienfeld JR, Brandt P, Brennicke A. The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nature Genet. 1997;15:57–61.
Vanlerberghe GC, Cvetkovska M, Wang J. Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? Physiol Plantarum. 2009;137:392–406.
Ward BL, Anderson RS, Bendich AJ. The mitochondrial genome is large and variable in a family of plants (Cucurbitaceae). Cell. 1981;25:793–803.
Woloszynska M. Heteroplasmy and stoichiometric complexity of plant mitochondrial genomes–though this be madness, yet there’s method in’t. J Exp Bot. 2010;61:657–71.
Zoubenko O, Allison L, Svab Z, Maliga P. Efficient targeting of foreign genes into the tobacco plastid genome. Nucleic Acids Res. 1994;22:3819–24.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Havey, M.J. (2016). Organellar Genomes of the Cucurbits. In: Grumet, R., Katzir, N., Garcia-Mas, J. (eds) Genetics and Genomics of Cucurbitaceae. Plant Genetics and Genomics: Crops and Models, vol 20. Springer, Cham. https://doi.org/10.1007/7397_2016_8
Download citation
DOI: https://doi.org/10.1007/7397_2016_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-49330-5
Online ISBN: 978-3-319-49332-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)