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American Society of Plant Biologists
A New Twist on TransposonsThe Maize Genome Harbors Helitron Insertion
News and Reviews Editor
Transposable elements (transposons or TEs), which are capable of transferring segments of DNA (or of being transferred) from one site to another within a genome, are abundant in eukaryotic genomes. The highly repetitive, largely noncoding sequence that is prevalent in eukaryotic genomes consists largely of TEs. TEs make up nearly half of the human genome (Lander et al., 2001
Until recently (Kapitonov and Jurka, 2001
Lal et al. (2003)  found the Helitron-like element within the Shrunken2 (Sh2) gene in the mutant sh2-7527, which appears to have arisen spontaneously in a conventional maize breeding program in the 1970s. sh2 mutants are characterized by kernels with poorly developed, shrunken endosperm tissue (Figure 1), resulting from mutations in the Sh2 gene, which encodes the large subunit of ADP-Glc pyrophosphorylase (Bhave et al., 1990). The Sh2 protein is a key enzyme in starch biosynthesis and is produced exclusively in the endosperm; sh2 mutants contain a much lower concentration of starch and a much higher concentration of Suc than the wild type. Because seed starch content is a major determinant of maize yields, characteri-zation of this locus has been of interest for many years (Tsai and Nelson, 1966; Smidansky et al., 2002).
Distinguishing features of the Helitrons identified by Kapitonov and Jurka (2001)
The Helitron-like insertion within the Sh2 gene of mutant sh2-7527 carries distinct hallmarks of Helitrons described by Kapitonov and Jurka (2001)
Current theory holds that the evolution of plant genomes is characterized by repeated rounds of large-scale genome duplication followed by selective gene loss (Ku et al., 2000 ; Gaut, 2001). In the maize genome, retrotransposon insertions appear to have brought about a doubling of genome size (from 1200 to 2400 Mb) within the last 3 million years (SanMiguel et al., 1998). Against the backdrop of these large-scale phenomena that have major impacts on overall genome structure and evolution, it is important to recognize that smaller events can have major evolutionary consequences. Helitrons have a number of features that suggest that they might be of considerable evolutionary importance. First is their possible role in gene duplications. Kapitonov and Jurka (2001) suggested that Helitrons might function as "powerful tools of evolution" by virtue of their apparent ability to recruit or "capture" host genes and multiply and modify them in the host genomes. The suggestion by Lal et al. that Helitrons may target transcriptionally active genes is particularly interesting in this regard. A second idea proposed by Kapitonov and Jurka (2001) is that geminiviruses (which appear to be limited to plants and which employ a rolling circle replication mechanism) evolved from plant Helitron transposons. Interestingly, integration of geminiviral DNA into the tobacco genome has been reported (Ashby et al., 1997). Thus, further investigation and analysis of plant Helitrons might lead to increased understanding of geminiviruses.
The estimate by Kapitonov and Jurka (2001) that Helitrons make up  2% of the Arabidopsis and Caenorhabditis genomes and are present in rice leads to the prediction that these elements exist in other plants as well as in other eukaryotes. Kapitonov and Jurka (2001) also concluded that Helitrons have been transposed "recently" in the rice genome (although this was not defined precisely) because a particular consensus sequence, called Helitron2_OS, was represented by two 15-kb copies that are 99% similar. The insertion in sh2-7527 is 12 kb and was found to be highly repetitive in maize in hybridization experiments. Thus, it is possible that autonomous as well as numerous nonautonomous copies of this element will be found eventually in the maize genome. It is also of interest that this particular element apparently multiplied in the maize genome after divergence from a common ancestor with its close relative sorghum, because hybridization with sorghum genomic DNA produced evidence of only one or two copies of the element.
The assertion that the nonautonomous sh2-7527 element was inserted very recently in the Sh2 gene rests on the assumption that this mutant arose in the 1970s. Maize mutant sh2 was described as early as 1949 (Mains, 1949
Ashby, M.K., Warry, A., Bejarano, E.R., Khashoggi, A., Burrell, M., and Lichtenstein, C.P. (1997). Analysis of multiple copies of geminiviral DNA in the genome of four closely related Nicotiana species suggest a unique integration event. Plant Mol. Biol. 35, 313–321.[ISI][Medline]
Bhave, M.R., Lawrence, S., Barton, C., and Hannah, L.C. (1990). Identification and molecular characterization of Shrunken-2 cDNA clones of maize. Plant Cell 2, 581–588.
Craig, N. (1995). Unity in transposition reactions. Science 270, 253–254. Feschotte, C., Jiang, N., and Wessler, S.R. (2002). Plant transposable elements: Where genetics meets genomics. Nat. Rev. Genet. 3, 329–341.[CrossRef][ISI][Medline]
Gaut, B.S. (2001). Patterns of chromosomal duplication in maize and their implications for comparative maps of the grasses. Genome Res. 11, 55–66.
Hannah, L.C., Tuschall, D.M., and Mans, R.J. (1980). Multiple forms of maize endosperm ADP-glucose pyrophosphorylase and their control by Shrunken-2 and Brittle-2. Genetics 95, 961–970.
Kapitonov, V.V., and Jurka, J. (2001). Rolling-circle transposons in eukaryotes. Proc. Natl. Acad. Sci. USA 98, 8714–8719.
Ku, H.-M., Vision, T., Liu, J., and Tanksley, S.D. (2000). Comparing sequenced segments of the tomato and Arabidopsis genomes: Large-scale duplication followed by selective gene loss creates a network of synteny. Proc. Natl. Acad. Sci. USA 97, 9121–9126.
Lal, S.K., Giroux, M.J., Brendel, V., Vallejos, C.E., and Hannah, L.C. (2003). The maize genome contains a Helitron insertion. Plant Cell 15, 381–391. Lander, E.S., et al. (2001). Initial sequencing and analysis of the human genome. Nature 409, 860–921.[CrossRef][Medline]
Mains, E.B. (1949). Heritable characters in maize: Linkage of a factor for shrunken endosperm with the A1 factor for aleurone color. J. Hered. 40, 21–24.
Meyers, B.C., Tingey, S.V., and Morgante, M. (2001). Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res. 11, 1660–1676. SanMiguel, P., Gaut, B.S., Tikhonov, A., Nakajima, Y., and Bennetzen, J.L. (1998). The paleontology of intergene retrotransposons of maize. Nat. Genet. 20, 43–45.[CrossRef][ISI][Medline]
Smidansky, E.D., Clancy, M., Meyer, F.D., Lanning, S.P., Blake, N.K., Talbert, L.E., and Giroux, M.J. (2002). Enhanced ADP-glucose pyrophosphorylase activity in wheat endosperm increases seed yield. Proc. Natl. Acad. Sci. USA 99, 1724–1729.
Tsai, C.Y., and Nelson, O.E. (1966). Starch deficient maize mutants lacking adenosine diphos-phate glucose pyrophosphorylase activity. Science 151, 341–343. Related articles in Plant Cell:
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