S-RNase-like Sequences in Styles of Coffea (Rubiaceae). Evidence for S-RNase Based Gametophytic Self-Incompatibility?

Although RNase-based self-incompatibility (SI) is suspected to operate in a wide group of plant families, it has been characterized as the molecular genetic basis of SI in only three distantly related families, Solanaceae, Plantaginaceae, and Rosaceae, all described over a decade ago. Previous studies found that gametophytic SI, controlled by a multi-allelic S-locus, operates in the coffee family (Rubiaceae). The molecular genetic basis of this mechanism remains unknown, despite the immense importance of coffee as an agricultural commodity. Here, we isolated ten sequences with features of T2-S-type RNases from two Coffea species. While three of the sequences were identified in both species and clearly do not appear to be S-locus products, our data suggest that six sequences may be S-alleles in the self-incompatible C. canephora, and one may be a relict in the self-compatible C. arabica. We demonstrate that these sequences show style-specific expression, display polymorphism in C. canephora, and cluster with S-locus products in a phylogenetic analysis that includes other plant families with RNase-based SI. Although our results are not definitive, in part because the available plant materials were limited and data patterns relatively complex, our results strongly hint that RNase-based SI mechanism operates in the Rubiaceae family.

[1]  M. Frohman,et al.  Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[2]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[3]  H. D. Niall,et al.  Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata , 1986, Nature.

[4]  P. Lashermes,et al.  Inheritance and genetic mapping of self-incompatibility in Coffea canephora Pierre , 1996, Theoretical and Applied Genetics.

[5]  K. Bawa,et al.  SELF‐INCOMPATIBILITY SYSTEMS IN THE RUBIACEAE OF A TROPICAL LOWLAND WET FOREST , 1983 .

[6]  Junli Zhou,et al.  The F-Box Protein AhSLF-S2 Controls the Pollen Function of S-RNase–Based Self-Incompatibility , 2004, The Plant Cell Online.

[7]  J. R. Lobry,et al.  SeqinR 1.0-2: A Contributed Package to the R Project for Statistical Computing Devoted to Biological Sequences Retrieval and Analysis , 2007 .

[8]  K. Holsinger,et al.  S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots. , 2002, Molecular biology and evolution.

[9]  H. Hirano,et al.  Structural and Transcriptional Analysis of the Self-Incompatibility Locus of Almond Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009290.: Identification of a Pollen-Expressed F-Box Gene with Haplotype-Specific Polymorphism , 2003, The Plant Cell Online.

[10]  A. Iezzoni,et al.  Identification and Characterization of S-RNases in Tetraploid Sour Cherry (Prunus cerasus) , 2001 .

[11]  David Posada,et al.  ProtTest: selection of best-fit models of protein evolution , 2005, Bioinform..

[12]  J. Golz,et al.  A molecular description of mutations affecting the pollen component of the Nicotiana alata S locus. , 1999, Genetics.

[13]  J. Stone Molecular Mechanisms Underlying The Breakdown Of Gametophytic Self‐incompatibility , 2002, The Quarterly Review of Biology.

[14]  S. Dussert,et al.  Molecular analysis of introgressive breeding in coffee (Coffea arabica L.) , 2000, Theoretical and Applied Genetics.

[15]  E. Coen,et al.  Origin of allelic diversity in antirrhinum S locus RNases. , 1996, The Plant cell.

[16]  S. Ho,et al.  Relaxed Phylogenetics and Dating with Confidence , 2006, PLoS biology.

[17]  J. Robert,et al.  Molecular characterisation and origin of the Coffea arabica L. genome , 1999, Molecular and General Genetics MGG.

[18]  J. Miller,et al.  Polyploidy and the evolution of gender dimorphism in plants. , 2000, Science.

[19]  M. Anderson,et al.  A relic S-RNase is expressed in the styles of self-compatible Nicotiana sylvestris. , 1998, The Plant journal : for cell and molecular biology.

[20]  Boris Igic,et al.  Evolutionary relationships among self-incompatibility RNases , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[21]  X. Argout,et al.  Coffee (Coffea arabica L.) genes early expressed during infection by the rust fungus (Hemileia vastatrix). , 2004, Molecular plant pathology.

[22]  E. Smets,et al.  Coffea (Rubiaceae) in Cameroon: a new species and a nomen recognized as species , 1996 .

[23]  S. Shafir,et al.  S-RNase based S-genotyping of Japanese plum (Prunus salicina Lindl.) and its implication on the assortment of cultivar-couples in the orchard , 2008 .

[24]  K. Osman,et al.  Investigating mechanisms involved in the self-incompatibility response in Papaver rhoeas. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[25]  R. Govaerts,et al.  An annotated taxonomic conspectus of the genus Coffea (Rubiaceae) , 2006 .

[26]  A. Iezzoni,et al.  Accumulation of Nonfunctional S-Haplotypes Results in the Breakdown of Gametophytic Self-Incompatibility in Tetraploid Prunus , 2006, Genetics.

[27]  J. Cairney,et al.  A simple and efficient method for isolating RNA from pine trees , 1993, Plant Molecular Biology Reporter.

[28]  R. DeSalle,et al.  Intron Evolution: Testing Hypotheses of Intron Evolution Using the Phylogenomics of Tetraspanins , 2009, PloS one.

[29]  J. Berthaud L'Incompatibilité chez Coffea canephora : méthode de test et déterminisme génétique , 1981 .

[30]  Robert C. Edgar,et al.  MUSCLE: a multiple sequence alignment method with reduced time and space complexity , 2004, BMC Bioinformatics.

[31]  Nuno A. Fonseca,et al.  An S-RNase-Based Gametophytic Self-Incompatibility System Evolved Only Once in Eudicots , 2008, Journal of Molecular Evolution.

[32]  D. Nettancourt Incompatibility in Angiosperms , 1977, Monographs on Theoretical and Applied Genetics.

[33]  G. D'alessio,et al.  Ribonucleases : structures and functions , 1997 .

[34]  Sudhir Kumar,et al.  MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers , 1994, Comput. Appl. Biosci..

[35]  H. Hirano,et al.  Identification and characterization of stylar glycoproteins associated with self-incompatibility genes of Japanese pear, Pyrus serotina Rehd , 1993, Molecular and General Genetics MGG.

[36]  U. Bastolla,et al.  Structural approaches to sequence evolution : molecules, networks, populations , 2007 .

[37]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[38]  A. Pallavicini,et al.  Differential responses of Coffea arabica L. leaves and roots to chemically induced systemic acquired resistance. , 2006, Genome.

[39]  S. Wright,et al.  The Distribution of Self-Sterility Alleles in Populations. , 1939, Genetics.

[40]  W. Broothaerts,et al.  Update on and Review of the Incompatibility (S-) Genotypes of , 2004 .

[41]  G. McFadden,et al.  Sequence variability of three alleles of the self-incompatibility gene of Nicotiana alata. , 1989, The Plant cell.

[42]  V. Su,et al.  Genetic analysis of Nicotiana pollen-part mutants is consistent with the presence of an S-ribonuclease inhibitor at the S locus , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[43]  B. Mable,et al.  Inheritance and dominance of self-incompatibility alleles in polyploid Arabidopsis lyrata , 2004, Heredity.

[44]  J. Huelsenbeck,et al.  SUCCESS OF PHYLOGENETIC METHODS IN THE FOUR-TAXON CASE , 1993 .

[45]  R. Lande,et al.  Loss of Self‐Incompatibility and Its Evolutionary Consequences , 2008, International Journal of Plant Sciences.

[46]  W. Heng,et al.  Competitive interaction between two functional S-haplotypes confer self-compatibility on tetraploid Chinese cherry (Prunus pseudocerasus Lindl. CV. Nanjing Chuisi) , 2008, Plant Cell Reports.

[47]  Shihshieh Huang,et al.  Identification of the pollen determinant of S-RNase-mediated self-incompatibility , 2004, Nature.

[48]  I. Coulibaly,et al.  Introgression of self-compatibility from Coffea heterocalyx to the cultivated species Coffea canephora , 2002, Theoretical and Applied Genetics.