Ethylene-Regulated Floral Volatile Synthesis in Petunia Corollas1[w]

In many flowering plants, such as petunia (Petunia × hybrida), ethylene produced in floral organs after pollination elicits a series of physiological and biochemical events, ultimately leading to senescence of petals and successful fertilization. Here, we demonstrate, using transgenic ethylene insensitive (44568) and Mitchell Diploid petunias, that multiple components of emission of volatile organic compounds (VOCs) are regulated by ethylene. Expression of benzoic acid/salicylic acid carboxyl methyltransferase (PhBSMT1 and 2) mRNA is temporally and spatially down-regulated in floral organs in a manner consistent with current models for postpollination ethylene synthesis in petunia corollas. Emission of methylbenzoate and other VOCs after pollination and exogenous ethylene treatment parallels a reduction in PhBSMT1 and 2 mRNA levels. Under cyclic light conditions (day/night), PhBSMT mRNA levels are rhythmic and precede emission of methylbenzoate by approximately 6 h. When shifted into constant dark or light conditions, PhBSMT mRNA levels and subsequent methylbenzoate emission correspondingly decrease or increase to minimum or maximum levels observed during normal conditions, thus suggesting that light may be a more critical influence on cyclic emission of methylbenzoate than a circadian clock. Transgenic PhBSMT RNAi flowers with reduced PhBSMT mRNA levels show a 75% to 99% decrease in methylbenzoate emission, with minimal changes in other petunia VOCs. These results implicate PhBSMT1 and 2 as genes responsible for synthesis of methylbenzoate in petunia.

[1]  Beverly A. Underwood,et al.  Circadian Regulation of the PhCCD1 Carotenoid Cleavage Dioxygenase Controls Emission of β-Ionone, a Fragrance Volatile of Petunia Flowers1 , 2004, Plant Physiology.

[2]  Beverly A. Underwood,et al.  The Central Role of PhEIN2 in Ethylene Responses throughout Plant Development in Petunia1 , 2004, Plant Physiology.

[3]  J. Tumlinson,et al.  The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. , 2004, The Plant journal : for cell and molecular biology.

[4]  Xinlu Chen,et al.  Understanding in Vivo Benzenoid Metabolism in Petunia Petal Tissue1 , 2004, Plant Physiology.

[5]  Richard A. Jorgensen,et al.  Chalcone synthase cosuppression phenotypes in petunia flowers: comparison of sense vs. antisense constructs and single-copy vs. complex T-DNA sequences , 1996, Plant Molecular Biology.

[6]  Beverly A. Underwood,et al.  Circadian Regulation of the PhCCD 1 Carotenoid Cleavage Dioxygenase Controls Emission of b-Ionone , a Fragrance Volatile of Petunia Flowers 1 , 2004 .

[7]  Feng Chen,et al.  An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. , 2003, The Plant journal : for cell and molecular biology.

[8]  Beverly A. Underwood,et al.  Regulation of Methylbenzoate Emission after Pollination in Snapdragon and Petunia Flowers Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016766. , 2003, The Plant Cell Online.

[9]  J. Tumlinson,et al.  Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Robert C Schuurink,et al.  Regulation of floral scent production in petunia revealed by targeted metabolomics. , 2003, Phytochemistry.

[11]  Beverly A. Underwood EFFECTS OF ETHYLENE ON FLORAL FRAGRANCE OF PETUNIA X HYBRIDA 'MITCHELL DIPLOID' , 2003 .

[12]  M. Holden,et al.  Pollination-induced ethylene promotes the early phase of pollen tube growth in Petunia inflata. , 2003, Journal of plant physiology.

[13]  B. Piechulla,et al.  Transcriptional and post-translational regulation of S-adenosyl-L-methionine: salicylic acid carboxyl methyltransferase (SAMT) during Stephanotis floribunda flower development. , 2003, Journal of plant physiology.

[14]  E. Pichersky,et al.  Evening specific oscillations of scent emission, SAMT enzyme activity, and SAMT mRNA in flowers of Stephanotis floribunda , 2002 .

[15]  C Robertson McClung,et al.  CIRCADIAN RHYTHMS IN PLANTS. , 2003, Annual review of plant physiology and plant molecular biology.

[16]  James H. Tumlinson,et al.  The influence of intact-plant and excised-leaf bioassay designs on volicitin- and jasmonic acid-induced sesquiterpene volatile release in Zea mays , 2001, Planta.

[17]  Natalia Dudareva,et al.  Regulation of Circadian Methyl Benzoate Emission in Diurnally and Nocturnally Emitting Plants , 2001, The Plant Cell Online.

[18]  P. Waterhouse,et al.  Construct design for efficient, effective and high-throughput gene silencing in plants. , 2001, The Plant journal : for cell and molecular biology.

[19]  N. Dudareva,et al.  Developmental Regulation of Methyl Benzoate Biosynthesis and Emission in Snapdragon Flowers , 2000, Plant Cell.

[20]  D. Clark,et al.  Reproduction and Horticultural Performance of Transgenic Ethylene-insensitive Petunias , 2000 .

[21]  H J Klee,et al.  Response to Xanthomonas campestris pv. vesicatoria in tomato involves regulation of ethylene receptor gene expression. , 2000, Plant physiology.

[22]  Michelle L. Jones,et al.  Interorgan Signaling following Pollination in Carnations , 1999 .

[23]  H. Klee,et al.  Root formation in ethylene-insensitive plants. , 1999, Plant physiology.

[24]  Harry T. Lawless,et al.  Sensory Evaluation of Food , 1999 .

[25]  Harro J. Bouwmeester,et al.  Circadian rhythmicity in emission of volatile compounds by flowers of Rosa hybrida L. cv. Honesty , 1998, Planta.

[26]  S. O'Neill,et al.  Three 1-aminocyclopropane-1-carboxylate synthase genes regulated by primary and secondary pollination signals in orchid flowers. , 1998, Plant physiology.

[27]  W. Doorn Effects of pollination on floral attraction and longevity. Review article , 1997 .

[28]  S. O'Neill POLLINATION REGULATION OF FLOWER DEVELOPMENT. , 1997, Annual review of plant physiology and plant molecular biology.

[29]  Elliot M. Meyerowitz,et al.  A dominant mutant receptor from Arabidopsis confers ethylene insensitivity in heterologous plants , 1997, Nature Biotechnology.

[30]  X. Tang,et al.  Temporal and Spatial Expression of 1-Aminocyclopropane-1-Carboxylate Oxidase mRNA following Pollination of Immature and Mature Petunia Flowers , 1996, Plant physiology.

[31]  L. Tollsten A multivariate approach to post-pollination changes in the floral scent of Platanthera bifolia (Orchidaceae) , 1993 .

[32]  J. Knudsen,et al.  Floral scents-a checklist of volatile compounds isolated by head-space techniques , 1993 .

[33]  X. S. Zhang,et al.  Interorgan regulation of ethylene biosynthetic genes by pollination. , 1993, The Plant cell.

[34]  F. Hoekstra,et al.  Lack of Control by Early Pistillate Ethylene of the Accelerated Wilting of Petunia hybrida Flowers. , 1986, Plant physiology.

[35]  D. E. Atkinson 3 – Functional Stoichiometric Coupling and Metabolic Prices* , 1977 .