Natural Variation as a Tool for Gene Identification in Plants

Abstract

The remarkable variety of plant form and adaptation observed in nature is genetically controlled, with input from environmental cues. Identifying the genes responsible for discrete as well as quantitative differences requires an understanding of the phenotypic and genetic diversity found among species. As opposed to gene cloning based on laboratory‚Äźinduced mutations, genes discovered through natural variation provide insight into the genetic mechanisms that drive evolutionary change of complex traits.

Keywords: phenotypic variation; allelic variation; natural diversity; qtl; domestication

Figure 1.

Diagram showing the step‐wise methodology of gene identification for quantitative traits through map‐based cloning. Starting from the top, each box describes a step in the process of gene identification. For qualitative variation based on single loci, an F2 population usually suffices, and the creation of a NIL is sometimes not necessary. Double arrows between ‘association mapping’ and ‘candidate gene’ indicate that QTL mapping can begin with an association mapping approach or a QTL can be verified with association mapping (see main text for details). Ultra‐high resolution involves the isolation of many recombinants in a small physical region surrounding the QTL. BAC – bacterial artificial chromosome library.

Figure 2.

Examples of genes underlying qualitative (a) and quantitative (b) natural variation in tomato. (a) The SELF PRUNING (SP) gene regulates flowering transition during sympodial growth in tomato. This naturally occurring mutant is the foundation of the processing tomato industry. Wild‐type ‘indeterminate’ plants (SP/−) initially flower (red balls) after five to eight leaves (green sticks), and then flower consecutively after every three leaves, indefinitely. Plants that are sp/sp mutants flower normally after five to eight leaves, but a‘determinate’ growth habit then ensues as flowering terminates, on average, after one fewer leaf following the preceding sympodium. This results in a shorter stature plant. Representatives of normal and mutant SP plants are shown next to each diagram. The SP gene has been cloned, revealing that a single base‐pair change is sufficient to qualitatively change tomato plant structure. SP, whose normal function is to suppress flowering similar to TERMINAL FLOWER (TFL) in Arabidopsis, is a member of a gene family involved in flowering transition, including ArabidopsisFT, which promotes flowering in a graft‐transmissible way and has been the target of natural variation for flowering time in rice. (b) Quantitative trait locus (QTL) mapping for fruit weight in tomato identified the fw2.2 locus as a major target of selection during the transition of wild tomato species from small fruits to the large‐fruited types that comprise present‐day cultivated tomato varieties. Near isogenic lines (NILs) that carry fw2.2 from the wild species S. pennellii can reduce fruit weight up to 30%, depending on the genetic background. The image shows representative fruit from an introgression line (IL), or large NIL, carrying three linked reducing fruit weight QTL from S. pennellii, the largest contributor of which is fw2.2 (top). Those plants without the introgression have larger fruits because they carry large‐fruited alleles of fw2.2 originating from cultivated S. lycopersicum (bottom). Fw2.2 was cloned and found to encode a hypothetical gene with putative structural similarity to oncogenic Ras proteins. The phenotypic change due to fw2.2 is based on genetic differences in upstream regulatory elements of the gene, as opposed to changes in coding sequence, which has become a recurring theme among genes identified through natural variation.

close

References

Alonso‐Blanco C, Mendez‐Vigo B and Koornneef M (2005) From phenotypic to molecular polymorphisms involved in naturally occurring variation of plant development. International Journal of Developmental Biology 49: 717–732.

Balasubramanian S, Sureshkumar S, Agrawal M et al. (2006) The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana. Nature Genetics 38: 711–715.

Doebley J, Stec A and Hubbard L (1997) The evolution of apical dominance in maize. Nature 386: 485–488.

Doebley J (2006) Plant science. Unfallen grains: how ancient farmers turned weeds into crops. Science 312: 1318–1319.

Doerge RW (2002) Mapping and analysis of quantitative trait loci in experimental populations. Nature Reviews Genetics 3: 43–52.

Manning K, Tor M, Poole M et al. (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP‐box transcription factor inhibits tomato fruit ripening. Nature Genetics 38: 948–952.

Martin GB, Bogdanove AJ and Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annual Review Plant Biology 54: 23–61.

Pnueli L, Carmel‐Goren L, Hareven D et al. (1998) The SELF‐PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125: 1979–1989.

Ronen G, Carmel‐Goren L, Zamir D and Hirschberg J (2000) An alternative pathway to beta‐carotene formation in plant chromoplasts discovered by map‐based cloning of beta and old‐gold color mutations in tomato. Proceedings of the National Academy of Sciences of the USA 97: 11102–11107.

Salvi S and Tuberosa R (2005) To clone or not to clone plant QTLs: present and future challenges. Trends in Plant Science 10: 297–304.

Tanksley SD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato.Plant Cell 16 (Suppl): S181–S189.

Further Reading

Ashikari M and Matsuoka M (2006) Identification, isolation and pyramiding of quantitative trait loci for rice breeding. Trends in Plant Science 11: 344–350.

Cardon LR and Bell JI (2001) Association study designs for complex diseases. Nature Reviews Genetics 2: 91–99.

Clark RM, Wagler TN, Quijada P and Doebley J (2006) A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nature Genetics 38: 594–597.

Diamond J (2002) Evolution, consequences and future of plant and animal domestication. Nature 418: 700–707.

Doebley J and Lukens L (1998) Transcriptional regulators and the evolution of plant form. Plant Cell 10: 1075–1082.

Fridman E, Carrari F, Liu YS, Fernie AR and Zamir D (2004) Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305: 1786–1789.

Henderson IR, Shindo C and Dean C (2003) The need for winter in the switch to flowering. Annual Review Genetics 37: 371–392.

Koornneef M, Alonso‐Blanco C and Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annual Review Plant Biology 55: 141–172.

Mitchell‐Olds T and Schmitt J (2006) Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441: 947–952.

Slate J (2005) Quantitative trait locus mapping in natural populations: progress, caveats and future directions. Molecular Ecology 14: 363–379.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Lippman, Zachary B, and Zamir, Dani(Jul 2007) Natural Variation as a Tool for Gene Identification in Plants. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020108]