Molecular Analysis of the anthocyanin2 Gene of Petunia and Its Role in the Evolution of Flower Color

The shape and color of flowers are important for plant reproduction because they attract pollinators such as insects and birds. Therefore, it is thought that alterations in these traits may result in the attraction of different pollinators, genetic isolation, and ultimately, (sympatric) speciation. Petunia integrifolia and P. axillaris bear flowers with different shapes and colors that appear to be visited by different insects. The anthocyanin2 (an2) locus, a regulator of the anthocyanin biosynthetic pathway, is the main determinant of color differences. Here, we report an analysis of molecular events at the an2 locus that occur during Petunia spp evolution. We isolated an2 by transposon tagging and found that it encodes a MYB domain protein, indicating that it is a transcription factor. Analysis of P. axillaris subspecies with white flowers showed that they contain an2- alleles with two alternative frameshifts at one site, apparently caused by the insertion and subsequent excision of a transposon. A third an2- allele has a nonsense mutation elsewhere, indicating that it arose independently. The distribution of polymorphisms in an2- alleles suggests that the loss of an2 function and the consequent changes in floral color were not the primary cause for genetic separation of P. integrifolia and P. axillaris. Rather, they were events that occurred late in the speciation process, possibly to reinforce genetic isolation and complete speciation.

[1]  A. van Houwelingen,et al.  Epigenetic Interactions among Three dTph1 Transposons in Two Homologous Chromosomes Activate a New Excision–Repair Mechanism in Petunia , 1999, Plant Cell.

[2]  S. W. Zhang,et al.  Honeybees link sights to smells , 1998, Nature.

[3]  C. Tonelli,et al.  Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[4]  J. Doebley,et al.  Transcriptional Regulators and the Evolution of Plant Form , 1998, Plant Cell.

[5]  V. Walbot,et al.  Functional Complementation of Anthocyanin Sequestration in the Vacuole by Widely Divergent Glutathione S-Transferases , 1998, Plant Cell.

[6]  E. Grotewold,et al.  How genes paint flowers and seeds , 1998 .

[7]  B. Weisshaar,et al.  Phenylpropanoid biosynthesis and its regulation. , 1998, Current opinion in plant biology.

[8]  C. Napoli,et al.  Psl: a novel Spm-like transposable element from Petunia hybrida. , 1998, The Plant journal : for cell and molecular biology.

[9]  M. Bliek,et al.  Genetic control of branching pattern and floral identity during Petunia inflorescence development. , 1998, Development.

[10]  J. Mol,et al.  Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. , 1998, The Plant journal : for cell and molecular biology.

[11]  A. van Houwelingen,et al.  Analysis of flower pigmentation mutants generated by random transposon mutagenesis in Petunia hybrida. , 1998, The Plant journal : for cell and molecular biology.

[12]  J. Mol,et al.  The an11 locus controlling flower pigmentation in petunia encodes a novel WD-repeat protein conserved in yeast, plants, and animals. , 1997, Genes & development.

[13]  J. Doebley,et al.  The evolution of apical dominance in maize , 1997, Nature.

[14]  E. Grotewold,et al.  Evidence for direct activation of an anthocyanin promoter by the maize C1 protein and comparison of DNA binding by related Myb domain proteins. , 1997, The Plant cell.

[15]  C. Martin,et al.  MYB transcription factors in plants. , 1997, Trends in genetics : TIG.

[16]  E. Grotewold,et al.  Differences between Plant and Animal Myb Domains Are Fundamental for DNA Binding Activity, and Chimeric Myb Domains Have Novel DNA Binding Specificities* , 1997, The Journal of Biological Chemistry.

[17]  C. Martin,et al.  Apparent redundancy in myb gene function provides gearing for the control of flavonoid biosynthesis in antirrhinum flowers. , 1996, The Plant cell.

[18]  A. van Hoof,et al.  Premature nonsense codons decrease the stability of phytohemagglutinin mRNA in a position-dependent manner. , 1996, The Plant journal : for cell and molecular biology.

[19]  M. Van Montagu,et al.  Insertion mutagenesis and study of transposable elements using a new unstable virescent seedling allele for isolation of haploid petunia lines. , 1996, The Plant Journal.

[20]  B. Gaut,et al.  Evolution of anthocyanin biosynthesis in maize kernels: the role of regulatory and enzymatic loci. , 1996, Genetics.

[21]  D. Schemske,et al.  Genetic mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus) , 1995, Nature.

[22]  T. Holton,et al.  Genetics and Biochemistry of Anthocyanin Biosynthesis. , 1995, The Plant cell.

[23]  V. Walbot,et al.  A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2 , 1995, Nature.

[24]  R. Koes,et al.  A general method to isolate genes tagged by a high copy number transposable element. , 1995, The Plant journal : for cell and molecular biology.

[25]  R. Solano,et al.  Dual DNA binding specificity of a petal epidermis‐specific MYB transcription factor (MYB.Ph3) from Petunia hybrida. , 1995, The EMBO journal.

[26]  Jonathan D. G. Jones,et al.  Altered regulation of tomato and tobacco pigmentation genes caused by the delila gene of Antirrhinum , 1995 .

[27]  H. Huits,et al.  Genetic control of dihydroflavonol 4-reductase gene expression in Petunia hybrida. , 1994, The Plant journal : for cell and molecular biology.

[28]  J. Mol,et al.  The flavonoid biosynthetic pathway in plants: Function and evolution , 1994 .

[29]  M. Bevan,et al.  A flower‐specific Myb protein activates transcription of phenylpropanoid biosynthetic genes. , 1994, The EMBO journal.

[30]  Yongbiao Xue,et al.  Cloning and structural analysis of the anthocyanin pigmentation locus Rt of Petunia hybrida: characterization of insertion sequences in two mutant alleles. , 1994, The Plant journal : for cell and molecular biology.

[31]  B. Burr,et al.  Maize anthocyanin regulatory gene pl is a duplicate of c1 that functions in the plant. , 1993, The Plant cell.

[32]  J. Mol,et al.  Regulatory Genes Controlling Anthocyanin Pigmentation Are Functionally Conserved among Plant Species and Have Distinct Sets of Target Genes. , 1993, The Plant cell.

[33]  C. Martin,et al.  Control of Pigment Biosynthesis Genes during Petal Development. , 1993, The Plant cell.

[34]  Ronald W. Davis,et al.  Arabidopsis and Nicotiana anthocyanin production activated by maize regulators R and C1. , 1992, Science.

[35]  S. Goff,et al.  Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. , 1992, Genes & development.

[36]  E. Coen,et al.  A common gene regulates pigmentation pattern in diverse plant species , 1992, Cell.

[37]  Jerry A. Coyne,et al.  Genetics and speciation , 1992, Nature.

[38]  Vickery,et al.  Pollinator preferences for yellow, orange, and red flowers of Mimulus verbenaceus and M. cardinalis , 1992 .

[39]  C. Martin,et al.  Control of anthocyanin biosynthesis in flowers of Antirrhinum majus. , 1991, The Plant journal : for cell and molecular biology.

[40]  E. Grotewold,et al.  Alternatively spliced products of the maize P gene encode proteins with homology to the DNA-binding domain of myb-like transcription factors. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[41]  J. Mol,et al.  Regulation and manipulation of flavonoid gene expression in anthers of petunia: the molecular basis of the Po mutation. , 1991, The Plant cell.

[42]  H. Huits,et al.  Molecular characterization of a nonautonomous transposable element (dTph1) of petunia. , 1990, The Plant cell.

[43]  S. Wessler,et al.  Maize R gene family: Tissue-specific helix-loop-helix proteins , 1990, Cell.

[44]  H. Saedler,et al.  The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto‐oncogene products and with structural similarities to transcriptional activators. , 1987, The EMBO journal.

[45]  E. Coen,et al.  Transposable elements generate novel spatial patterns of gene expression in antirrhinum majus , 1986, Cell.

[46]  H. Saedler,et al.  Plant Transposable Elements , 1986 .

[47]  H. Wijsman.  ON THE INTERRELATIONSHIPS OF CERTAIN SPECIES OF PETUNIA II. EXPERIMENTAL DATA: CROSSES BETWEEN DIFFERENT TAXA , 1983 .

[48]  H. Wijsman.  ON THE INTERRELATIONSHIPS OF CERTAIN SPECIES OF PETUNIA , 1982 .

[49]  A. Cornu.  Systemes instables induits chez le petunia , 1977 .