PHYSIOLOGICAL AND MOLECULAR CHANGES DURING OPENING AND SENESCENCE OF NICOTIANA MUTABILIS FLOWERS

Authors: MACNISH, ANDREW - University Of California; NEGRE-ZAKHAROV, FLORENCE - University Of California; Jiang, Cai-Zhong; REID, MICHAEL - University Of California

Submitted to: Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/26/2010
Publication Date: 1/1/2010
Citation: Macnish, A.J., Negre-Zakharov, F., Jiang, C., Reid, M.S. 2010. PHYSIOLOGICAL AND MOLECULAR CHANGES DURING OPENING AND SENESCENCE OF NICOTIANA MUTABILIS FLOWERS. Plant Science. 179:267-272.

Interpretive Summary: Flower senescence is a complex metabolic process under strict control by developmental and environmental signals. Visible as wilting and/or fading of floral organs, senescence is preceded and accompanied by extensive degradation of nucleic acids, proteins and membranes. It is also associated with considerable changes in gene transcription and translation. A number of senescence-associated genes (SAGs) encode catabolic enzymes such as proteases and nucleases. Proteases regulate metabolic and developmental processes by facilitating turnover of rate-limiting proteins. Cysteine proteases appear to play a particularly important role in senescence as they are consistently identified in senescing floral tissues. Among the cysteine proteases, SAG12 has been most closely related to senescence. Transcripts of SAG12 are only detected at the onset of visible senescence in Arabidopsis leaves and tobacco flowers. Thus, SAG12 may represent a useful and specific marker for the study of floral senescence. The phytohormone ethylene is the primary regulator of floral senescence in a wide range of plant genera. In sensitive species, petal senescence is associated with an increase in endogenous ethylene production, while exposure to exogenous ethylene greatly accelerates the process. Moreover, treatment with inhibitors of ethylene biosynthesis and action delay flower senescence. Studies with species such as carnation, daffodil and petunia have revealed that ethylene coordinates and enhances expression of several floral senescence-associated cysteine proteases. A close relative of tobacco, Nicotiana mutabilis, was recently discovered in southern Brazil. As its specific epithetic suggests, the petals of N. mutabilis change in colour from white through pink to red as the flowers age. Although changes in colour are associated with floral senescence in a range of other species (Cichorium intybus, Lupinus perennis, Desmodium setigerum, Gossypium hirsutum) these species are not as nearly well-studied at the molecular level as species of tobacco. Emission of fragrant volatiles, namely 1,8-cineole and linalool, were also found to increase by 2- to 9-fold as N. mutabilis petals developed pink colouration. Pollination of flowers was reported to reduce their longevity, suggesting that ethylene may regulate flower senescence. By virtue of its close relationship to the model plant tobacco, a range of genetic tools would also be available for the study of N. mutabilis flowers. Accordingly, N. mutabilis potentially represents an interesting alternative system for molecular studies of ethylene-mediated flower senescence. We characterized physiological and molecular changes during opening and senescence of N. mutabilis flowers. The flowers of Nicotiana mutabilis have petals that undergo a striking colour change from white through pink to red as they open and senesce over a typical 7-d lifespan. Colouration in petals was associated with an increase in chalcone synthase (CHS) gene expression and a substantial rise in the anthocyanin content. It was also initially accompanied by up-regulation of 1- aminocyclopropane-1-carboxylic acid oxidase (ACO) transcripts and consequently by elevated rates of ethylene production at the onset of petal wilting. Emission of the fragrant monoterpenoid volatiles 1,8-cineole, linalool and terpineol also increased as petals developed pink colouration. The increase in volatile emission was preceded by a rise in monoterpene synthase (MTS) gene expression in petals. Transcripts of a homolog of SAG12, a senescence-associated gene encoding a cysteine protease, began to accumulate in petals 3 d prior to visible wilting as the colour change advanced and ethylene production increased. Exposure of newly opened white flowers to 1 µl l-1 ethylene accelerated petal colouration, wilting, and induction of SAG12 expression by ca.

Technical Abstract: The flowers of Nicotiana mutabilis, a tobacco species recently discovered in southern Brazil, have petals that undergo a striking colour change from white through pink to red as they open and senesce over a typical 7-d lifespan. Colouration in petals was associated with an increase in chalcone synthase (CHS) gene expression and a substantial rise in the anthocyanin content. It was also initially accompanied by up-regulation of 1- aminocyclopropane-1-carboxylic acid oxidase (ACO) transcripts and consequently by elevated rates of ethylene production at the onset of petal wilting. Emission of the fragrant monoterpenoid volatiles 1,8-cineole, linalool and terpineol also increased as petals developed pink colouration. The increase in volatile emission was preceded by a rise in monoterpene synthase (MTS) gene expression in petals. Transcripts of a homolog of SAG12, a senescence-associated gene encoding a cysteine protease, began to accumulate in petals 3 d prior to visible wilting as the colour change advanced and ethylene production increased. Exposure of newly opened white flowers to 1 µl l-1 ethylene accelerated petal colouration, wilting, and induction of SAG12 expression by ca. 1 d while treatment with 500 nl l-1 1-methylcyclopropene (1-MCP), an inhibitor of ethylene action, retarded these processes. The numerous genetic and experimental tools available for tobacco can readily be applied to this close relative, which therefore provides an interesting new model for studying ethylene-mediated flower senescence.