Outstanding questions in flower metabolism.
Fusarium
canalization
flower development
flower metabolism
nectar
nitrogen
pollination
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
13
03
2020
revised:
29
04
2020
accepted:
05
05
2020
pubmed:
16
5
2020
medline:
2
3
2021
entrez:
16
5
2020
Statut:
ppublish
Résumé
The great diversity of flowers, their color, odor, taste, and shape, is mostly a result of the metabolic processes that occur in this reproductive organ when the flower and its tissues develop, grow, and finally die. Some of these metabolites serve to advertise flowers to animal pollinators, other confer protection towards abiotic stresses, and a large proportion of the molecules of the central metabolic pathways have bioenergetic and signaling functions that support growth and the transition to fruits and seeds. Although recent studies have advanced our general understanding of flower metabolism, several questions still await an answer. Here, we have compiled a list of open questions on flower metabolism encompassing molecular aspects, as well as topics of relevance for agriculture and the ecosystem. These questions include the study of flower metabolism through development, the biochemistry of nectar and its relevance to promoting plant-pollinator interaction, recycling of metabolic resources after flowers whiter and die, as well as the manipulation of flower metabolism by pathogens. We hope with this review to stimulate discussion on the topic of flower metabolism and set a reference point to return to in the future when assessing progress in the field.
Substances chimiques
Plant Nectar
0
Nitrogen
N762921K75
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1275-1288Informations de copyright
© 2020 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Abolmaali, S., Mitterbauer, R., Spadiut, O., Peruci, M., Weindorfer, H., Lucyshyn, D., Ellersdorfer, G., Lemmens, M., Moll, W.D. and Adam, G. (2008) Engineered bakers yeast as a sensitive bioassay indicator organism for the trichothecene toxin deoxynivalenol. J. Microbiol. Methods, 72, 306-312.
Adebesin, F., Widhalm, J.R., Boachon, B., Lefèvre, F., Pierman, B., Lynch, J.H., Alam, I., Junqueira, B., Benke, R. and Ray, S. (2017) Emission of volatile organic compounds from petunia flowers is facilitated by an ABC transporter. Science (New York, N.Y.), 356, 1386-1388.
Adebesin, F., Widhalm, J.R., Lynch, J.H., McCoy, R.M. and Dudareva, N. (2018) A peroxisomal thioesterase plays auxiliary roles in plant β-oxidative benzoic acid metabolism. Plant J. 93, 905-916.
Ali, Z., Mahfouz, M.M. and Mansoor, S. (2020) CRISPR-TSKO: a tool for tissue-specific genome editing in plants. Trends Plant Sci. 25, 123-126.
Alseekh, S., Tong, H., Scossa, F., Brotman, Y., Vigroux, F., Tohge, T., Ofner, I., Zamir, D., Nikoloski, Z. and Fernie, A.R. (2017) Canalization of tomato fruit metabolism. Plant Cell, 29, 2753-2765.
Armbruster, W.S. and Wege, J.A. (2019) Detecting canalization and intra-floral modularity in triggerplant (Stylidium) flowers: correlations are only part of the story. Ann. Bot. 123, 355-372.
Avin-Wittenberg, T., Bajdzienko, K., Wittenberg, G., Alseekh, S., Tohge, T., Bock, R., Giavalisco, P. and Fernie, A.R. (2015) Global analysis of the role of autophagy in cellular metabolism and energy homeostasis in Arabidopsis seedlings under carbon starvation. Plant Cell, 27, 306-322.
Babst, B.A., Gao, F., Acosta-Gamboa, L.M., Karve, A., Schueller, M.J. and Lorence, A. (2019) Three NPF genes in Arabidopsis are necessary for normal nitrogen cycling under low nitrogen stress. Plant Physiol. Biochem. 143, 1-10.
Bailes, E.J., Ollerton, J., Pattrick, J.G. and Glover, B.J. (2015) How can an understanding of plant-pollinator interactions contribute to global food security? Curr. Opin. Plant Biol. 26, 72-79.
Bellaire, A., Ischebeck, T., Staedler, Y., Weinhaeuser, I., Mair, A., Parameswaran, S., Ito, T., Schönenberger, J. and Weckwerth, W. (2014) Metabolism and development-integration of micro computed tomography data and metabolite profiling reveals metabolic reprogramming from floral initiation to silique development. New Phytol. 202, 322-335.
Berg, R. (1960) The ecological significance of correlation pleiades. Evolution, 14, 171-180.
Bertheloot, J., Cournède, P.-H. and Andrieu, B. (2011) NEMA, a functional-structural model of nitrogen economy within wheat culms after flowering. I. Model description. Ann. Bot. 108, 1085-1096.
Bieleski, R.L. (1995) Onset of phloem export from senescent petals of daylily. Plant Physiol. 109, 557-565.
Bolton, M.D. and Thomma, B.P. (2008) The complexity of nitrogen metabolism and nitrogen-regulated gene expression in plant pathogenic fungi. Physiol. Mol. Plant Pathol. 72, 104-110.
Borghi, M. and Fernie, A.R. (2017) Floral metabolism of sugars and amino acids: implications for pollinators' preferences and seed and fruit set. Plant Physiol. 175, 1510-1524.
Borghi, M., Fernie, A.R., Schiestl, F.P. and Bouwmeester, H.J. (2017) The sexual advantage of looking, smelling, and tasting good: the metabolic network that produces signals for pollinators. Trends Plant Sci. 22, 338-350.
Borghi, M., Perez de Souza, L., Yoshida, T. and Fernie, A.R. (2019) Flowers and climate change: a metabolic perspective. New Phytol. 224, 1425-1441.
Brandoli, C., Petri, C., Egea-Cortines, M. and Weiss, J. (2020) The clock gene Gigantea 1 from Petunia hybrida coordinates vegetative growth and inflorescence architecture. Sci. Rep. 10, 1-17.
Brazel, A.J. and Ó'Maoiléidigh, D.S. (2019) Photosynthetic activity of reproductive organs. Oxford, UK: Oxford University Press.
Cardon, Z.G., Stark, J.M., Herron, P.M. and Rasmussen, J.A. (2013) Sagebrush carrying out hydraulic lift enhances surface soil nitrogen cycling and nitrogen uptake into inflorescences. Proc. Natl Acad. Sci. 110, 18988-18993.
Cardoso-Gustavson, P. and Davis, A. (2015) Is nectar reabsorption restricted by the stalk cells of floral and extrafloral nectary trichomes? Plant Biol. 17, 134-146.
Cellini, A., Giacomuzzi, V., Donati, I., Farneti, B., Rodriguez-Estrada, M.T., Savioli, S., Angeli, S. and Spinelli, F. (2019) Pathogen-induced changes in floral scent may increase honeybee-mediated dispersal of Erwinia amylovora. ISME J. 13, 847-859.
Chai, T.-T., Simmonds, D., Day, D.A., Colmer, T.D. and Finnegan, P.M. (2010) Photosynthetic performance and fertility are repressed in GmAOX2b antisense soybean. Plant Physiol. 152, 1638-1649.
Chatt, E.C., Mahalim, S.-N., Mohd-Fadzil, N.-A., Roy, R., Klinkenberg, P.M., Horner, H.T., Hampton, M., Carter, C.J. and Nikolau, B.J. (2019) Systems analyses of key metabolic modules of floral and extrafloral nectaries of cotton. BioRxiv, 857771.
Chatt, E.C., von Aderkas, P., Carter, C.J., Smith, D., Elliott, M. and Nikolau, B.J. (2018) Sex-dependent variation of pumpkin (Cucurbita maxima cv. Big Max) nectar and nectaries as determined by proteomics and metabolomics. Front. Plant Sci., 9, 860.
Chen, D., Yan, W., Fu, L.-Y. and Kaufmann, K. (2018) Architecture of gene regulatory networks controlling flower development in Arabidopsis thaliana. Nat. Commun. 9, 1-13.
Christmann, S. (2019) Climate change enforces to look beyond the plant - the example of pollinators. Curr. Opin. Plant Biol. https://doi.org/10.1016/j.pbi.2019.11.001.
Cna'ani, A., Spitzer-Rimon, B., Ravid, J., Farhi, M., Masci, T., Aravena-Calvo, J., Ovadis, M. and Vainstein, A. (2015) Two showy traits, scent emission and pigmentation, are finely coregulated by the MYB transcription factor PH 4 in petunia flowers. New Phytol. 208, 708-714.
Conner, J.K. and Lande, R. (2014) Raissa L. Berg's contributions to the study of phenotypic integration, with a professional biographical sketch. Philosophical Transactions of the Royal Society B: Biological Sciences, 369, 20130250.
Cuperlovic-Culf, M., Vaughan, M.M., Vermillion, K., Surendra, A., Teresi, J. and McCormick, S.P. (2019) Effects of atmospheric CO2 level on the metabolic response of resistant and susceptible wheat to Fusarium graminearum infection. Mol. Plant Microbe Interact. 32, 379-391.
Daloso, D.M., Medeiros, D.B., Dos Anjos, L., Yoshida, T., Araújo, W.L. and Fernie, A.R. (2017) Metabolism within the specialized guard cells of plants. New Phytol. 216, 1018-1033.
Darwin, C. (1877) The Different Forms of Flowers on Plants of the Same Species. London, UK: John Murray.
de Ibarra, N.H., Langridge, K.V. and Vorobyev, M. (2015) More than colour attraction: behavioural functions of flower patterns. Curr. Opin. Insect Sci. 12, 64-70.
de Souza Chaves, I., Feitosa-Araujo, E., Florian, A. et al. (2019) The mitochondrial NAD(+) transporter (NDT1) plays important roles in cellular NAD(+) homeostasis in Arabidopsis thaliana. Plant J. 100, 487-504.
Dean, R., Van Kan, J.A., Pretorius, Z.A., Hammond-Kosack, K.E., Di Pietro, A., Spanu, P.D., Rudd, J.J., Dickman, M., Kahmann, R. and Ellis, J. (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13, 414-430.
Decourtye, A., Alaux, C., Le Conte, Y. and Henry, M. (2019) Toward the protection of bees and pollination under global change: present and future perspectives in a challenging applied science. Curr. Opin. Insect Sci. 35, 123-131.
Del-Saz, N.F., Ribas-Carbo, M., McDonald, A.E., Lambers, H., Fernie, A.R. and Florez-Sarasa, I. (2018) An in vivo perspective of the role (s) of the alternative oxidase pathway. Trends Plant Sci. 23, 206-219.
Descamps, C., Quinet, M., Baijot, A. and Jacquemart, A.L. (2018) Temperature and water stress affect plant-pollinator interactions in Borago officinalis (Boraginaceae). Ecol. Evol. 8, 3443-3456.
Ding, B., Patterson, E.L., Holalu, S.V., Li, J., Johnson, G.A., Stanley, L.E., Greenlee, A.B., Peng, F., Bradshaw, H. Jr and Blinov, M.L. (2020) Two myb proteins in a self-organizing activator-inhibitor system produce spotted pigmentation patterns. Curr. Biol. 30, 802-814.e8.
Djamei, A., Schipper, K., Rabe, F., Ghosh, A., Vincon, V., Kahnt, J., Osorio, S., Tohge, T., Fernie, A.R. and Feussner, I. (2011) Metabolic priming by a secreted fungal effector. Nature, 478, 395-398.
Doehlemann, G., Wahl, R., Horst, R.J., Voll, L.M., Usadel, B., Poree, F., Stitt, M., Pons-Kühnemann, J., Sonnewald, U. and Kahmann, R. (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J. 56, 181-195.
Donati, I., Cellini, A., Buriani, G., Mauri, S., Kay, C., Tacconi, G. and Spinelli, F. (2018) Pathways of flower infection and pollen-mediated dispersion of Pseudomonas syringae pv. actinidiae, the causal agent of kiwifruit bacterial canker. Hortic. Res. 5, 1-13.
Doppler, M., Kluger, B., Bueschl, C., Steiner, B., Buerstmayr, H., Lemmens, M., Krska, R., Adam, G. and Schuhmacher, R. (2019) Stable isotope-assisted plant metabolomics: investigation of phenylalanine-related metabolic response in wheat upon treatment with the fusarium virulence factor deoxynivalenol. Front. Plant Sci. 10, 1137.
Dowell, J.A., Reynolds, E.C., Pliakas, T.P., Mandel, J.R., Burke, J.M., Donovan, L.A. and Mason, C.M. (2019) Genome-wide association mapping of floral traits in cultivated sunflower (Helianthus annuus). J. Hered. 110, 275-286.
Duan, Q., Kita, D., Johnson, E.A., Aggarwal, M., Gates, L., Wu, H.M. and Cheung, A.Y. (2014) Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat. Commun. 5, 3129.
Fagard, M., Launay, A., Clément, G., Courtial, J., Dellagi, A., Farjad, M., Krapp, A., Soulié, M.-C. and Masclaux-Daubresse, C. (2014) Nitrogen metabolism meets phytopathology. J. Exp. Bot. 65, 5643-5656.
Farkas, A., Mihalik, E., Dorgai, L. and Bubán, T. (2012) Floral traits affecting fire blight infection and management. Trees, 26, 47-66.
Fenske, M.P., Hazelton, K.D.H., Hempton, A.K., Shim, J.S., Yamamoto, B.M., Riffell, J.A. and Imaizumi, T. (2015) Circadian clock gene LATE ELONGATED HYPOCOTYL directly regulates the timing of floral scent emission in Petunia. Proc. Natl Acad. Sci. 112, 9775-9780.
Fernie, A.R. and Schauer, N. (2009) Metabolomics-assisted breeding: a viable option for crop improvement? Trends Genet. 25, 39-48.
Fischer, W.-N., Kwart, M., Hummel, S. and Frommer, W.B. (1995) Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. J. Biol. Chem. 270, 16315-16320.
Fornoff, F., Klein, A.M., Hartig, F., Benadi, G., Venjakob, C., Schaefer, H.M. and Ebeling, A. (2017) Functional flower traits and their diversity drive pollinator visitation. Oikos, 126, 1020-1030.
Gaufichon, L., Marmagne, A., Belcram, K. et al. (2017) ASN1-encoded asparagine synthetase in floral organs contributes to nitrogen filling in Arabidopsis seeds. Plant J. 91, 371-393.
Givnish, T.J. (2002) Ecological constraints on the evolution of plasticity in plants. Evol. Ecol. 16, 213-242.
Goetz, M., Guivarch, A., Hirsche, J. et al. (2017) Metabolic control of tobacco pollination by sugars and invertases. Plant Physiol. 173, 984-997.
Goto-Yamada, S., Mano, S. and Nishimura, M. (2014) The role of peroxisomes in plant reproductive processes. In Sexual Reproduction in Animals and Plants (Sawada, H., Inoue, N. and Iwano, M., eds). Berlin, Germany: Springer-Verlag GmbH, pp. 419-429.
Goulet, K.M. and Saville, B.J. (2017) Carbon acquisition and metabolism changes during fungal biotrophic plant pathogenesis: insights from Ustilago maydis. Can. J. Plant Pathol. 39, 247-266.
Grafahrend-Belau, E., Junker, A., Eschenröder, A., Müller, J., Schreiber, F. and Junker, B.H. (2013) Multiscale metabolic modeling: dynamic flux balance analysis on a whole-plant scale. Plant Physiol. 163, 637-647.
Guerrero-Rubio, M.A., Escribano, J., García-Carmona, F. and Gandía-Herrero, F. (2019) Light emission in betalains: from fluorescent flowers to biotechnological applications. Trends Plant Sci. 25, 159-175.
Guiboileau, A., Avila-Ospina, L., Yoshimoto, K., Soulay, F., Azzopardi, M., Marmagne, A., Lothier, J. and Masclaux-Daubresse, C. (2013) Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability. New Phytol. 199, 683-694.
Hammes, U.Z., Nielsen, E., Honaas, L.A., Taylor, C.G. and Schachtman, D.P. (2006) AtCAT6, a sink-tissue-localized transporter for essential amino acids in Arabidopsis. Plant J. 48, 414-426.
Hay, A.S., Pieper, B., Cooke, E., Mandakova, T., Cartolano, M., Tattersall, A.D., Ioio, R.D., McGowan, S.J., Barkoulas, M. and Galinha, C. (2014) Cardamine hirsuta: a versatile genetic system for comparative studies. Plant J. 78, 1-15.
Higashiyama, T. and Yang, W.-C. (2017) Gametophytic pollen tube guidance: attractant peptides, gametic controls, and receptors. Plant Physiol. 173, 112-121.
Horst, R.J., Doehlemann, G., Wahl, R., Hofmann, J., Schmiedl, A., Kahmann, R., Kämper, J., Sonnewald, U. and Voll, L.M. (2010) Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiol. 152, 293-308.
Ishihara, H., Moraes, T.A., Pyl, E.T., Schulze, W.X., Obata, T., Scheffel, A., Fernie, A.R., Sulpice, R. and Stitt, M. (2017) Growth rate correlates negatively with protein turnover in Arabidopsis accessions. Plant J. 91, 416-429.
Ito-Inaba, Y., Sato, M., Sato, M.P., Kurayama, Y., Yamamoto, H., Ohata, M., Ogura, Y., Hayashi, T., Toyooka, K. and Inaba, T. (2019) Alternative oxidase capacity of mitochondria in microsporophylls may function in cycad thermogenesis. Plant Physiol. 180, 743-756.
Jiao, J., Mizukami, A.G., Sankaranarayanan, S., Yamguchi, J., Itami, K. and Higashiyama, T. (2017) Structure-activity relation of AMOR sugar molecule that activates pollen-tubes for ovular guidance. Plant Physiol. 173, 354-363.
Johnson, M.A., Harper, J.F. and Palanivelu, R. (2019) A fruitful journey: pollen tube navigation from germination to fertilization. Annu. Rev. Plant Biol. 70, 809-837.
Jones, M.L. (2013) Mineral nutrient remobilization during corolla senescence in ethylene-sensitive and-insensitive flowers. AoB Plants, 5, plt023.
Joseph, B., Corwin, J.A. and Kliebenstein, D.J. (2015) Genetic variation in the nuclear and organellar genomes modulates stochastic variation in the metabolome, growth, and defense. PLoS Genet. 11, e1004779.
Kanno, A. (2015) Molecular mechanism regulating floral architecture in monocotyledonous ornamental plants. Hortic J. MI-IR05.
Kim, Y.-J., Zhang, D. and Jung, K.-H. (2019) Molecular basis of pollen germination in cereals. Trends Plant Sci. 24, 1126-1136.
Kishor, K., Polavarapu, B., Hima Kumari, P., Sunita, M. and Sreenivasulu, N. (2015) Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Front. Plant Sci. 6, 544.
Klein, A.-M., Vaissiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C. and Tscharntke, T. (2007) Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B. Biol. Sci. 274, 303-313.
Knutsen, H.K., Alexander, J., Barregård, L., Bignami, M., Brüschweiler, B., Ceccatelli, S., Cottrill, B., Dinovi, M. and Grasl-Kraupp, B. (2017) Risks to human and animal health related to the presence of deoxynivalenol and its acetylated and modified forms in food and feed. EFSA J. 15, e04718.
Komarova, N.Y., Thor, K., Gubler, A., Meier, S., Dietrich, D., Weichert, A., Suter Grotemeyer, M., Tegeder, M. and Rentsch, D. (2008) AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiol. 148, 856-869.
Kretschmer, M., Croll, D. and Kronstad, J.W. (2017) Maize susceptibility to Ustilago maydis is influenced by genetic and chemical perturbation of carbohydrate allocation. Mol. Plant Pathol. 18, 1222-1237.
Kwak, M.S., Min, S.R., Lee, S.-M., Kim, K.-N., Liu, J.R., Paek, K.-H., Shin, J.S. and Bae, J.M. (2007) A sepal-expressed ADP-glucose pyrophosphorylase gene (NtAGP) is required for petal expansion growth in ‘Xanthi’ tobacco. Plant Physiol. 145, 277-289.
Laitinen, R.A. and Nikoloski, Z. (2019) Genetic basis of plasticity in plants. J. Exp. Bot. 70, 739-745.
Lee, Y.H. and Tegeder, M. (2004) Selective expression of a novel high-affinity transport system for acidic and neutral amino acids in the tapetum cells of Arabidopsis flowers. Plant J. 40, 60-74.
Li, B., Zhang, Y., Mohammadi, S.A., Huai, D., Zhou, Y. and Kliebenstein, D.J. (2016a) An integrative genetic study of rice metabolism, growth and stochastic variation reveals potential C/N partitioning loci. Sci. Rep. 6, 30143.
Li, D., Heiling, S., Baldwin, I.T. and Gaquerel, E. (2016b) Illuminating a plant’s tissue-specific metabolic diversity using computational metabolomics and information theory. Proc. Natl Acad. Sci. 113, E7610-E7618.
Lin, I.W., Sosso, D., Chen, L.-Q., Gase, K., Kim, S.-G., Kessler, D., Klinkenberg, P.M., Gorder, M.K., Hou, B.-H. and Qu, X.-Q. (2014) Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature, 508, 546-549.
Liu, Q., Galli, M., Liu, X., Federici, S., Buck, A., Cody, J., Labra, M. and Gallavotti, A. (2019) NEEDLE1 encodes a mitochondria localized ATP-dependent metalloprotease required for thermotolerant maize growth. Proc. Natl Acad. Sci. 116, 19736-19742.
Lopes, A.L., Moreira, D., Ferreira, M.J., Pereira, A.M. and Coimbra, S. (2019) Insights into secrets along the pollen tube pathway in need to be discovered. J. Exp. Bot. 70, 2979-2992.
Luyt, R. and Johnson, S. (2002) Postpollination nectar reabsorption and its implications for fruit quality in an epiphytic orchid1. Biotropica, 34, 442-446.
Lynch, J.H., Qian, Y., Guo, L., Maoz, I., Huang, X.-Q., Garcia, A.S., Louie, G., Bowman, M.E., Noel, J.P. and Morgan, J.A. (2020) Modulation of auxin formation by the cytosolic phenylalanine biosynthetic pathway. Nat. Chem. Biol. 1-7. https://doi.org/10.1038/s41589-020-0519-8
Ma, G., Shi, X., Zou, Q., Tian, D., An, X. and Zhu, K. (2018) iTRAQ-based quantitative proteomic analysis reveals dynamic changes during daylily flower senescence. Planta, 248, 859-873.
Magnard, J.-L., Roccia, A., Caissard, J.-C., Vergne, P., Sun, P., Hecquet, R., Dubois, A., Hibrand-Saint Oyant, L., Jullien, F. and Nicolè, F. (2015) Biosynthesis of monoterpene scent compounds in roses. Science (New York, N.Y.), 349, 81-83.
Matile, P. and Winkenbach, F. (1971) Function of lysosomes and lysosomal enzymes in the senescing corolla of the morning glory (Ipomoea purpurea). J. Exp. Bot. 22, 759-771.
McArt, S.H., Koch, H., Irwin, R.E. and Adler, L.S. (2014) Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens. Ecol. Lett. 17, 624-636.
McKim, S.M., Routier-Kierzkowska, A.-L., Monniaux, M., Kierzkowski, D., Pieper, B., Smith, R.S., Tsiantis, M. and Hay, A. (2017) Seasonal regulation of petal number. Plant Physiol. 175, 886-903.
Mellema, S., Eichenberger, W., Rawyler, A., Suter, M., Tadege, M. and Kuhlemeier, C. (2002) The ethanolic fermentation pathway supports respiration and lipid biosynthesis in tobacco pollen. Plant J. 30, 329-336.
Meng, Y., Wang, Z., Wang, Y., Wang, C., Zhu, B., Liu, H., Ji, W., Wen, J., Chu, C. and Tadege, M. (2019) The MYB activator WHITE PETAL1 associates with MtTT8 and MtWD40-1 to regulate carotenoid-derived flower pigmentation in Medicago truncatula. Plant Cell, 31, 2751-2767.
Miyazawa, H. and Aulehla, A. (2018) Revisiting the role of metabolism during development. Development, 145, dev131110.
Muhlemann, J.K., Maeda, H., Chang, C.-Y., San Miguel, P., Baxter, I., Cooper, B., Perera, M.A., Nikolau, B.J., Vitek, O. and Morgan, J.A. (2012) Developmental changes in the metabolic network of snapdragon flowers. PLoS ONE, 7, e40381.
Müller, G.L., Drincovich, M.F., Andreo, C.S. and Lara, M.V. (2010) Role of photosynthesis and analysis of key enzymes involved in primary metabolism throughout the lifespan of the tobacco flower. J. Exp. Bot. 61, 3675-3688.
Mur, L.A., Simpson, C., Kumari, A., Gupta, A.K. and Gupta, K.J. (2017) Moving nitrogen to the centre of plant defence against pathogens. Ann. Bot. 119, 703-709.
Nakamura, Y., Teo, N.Z., Shui, G., Chua, C.H., Cheong, W.F., Parameswaran, S., Koizumi, R., Ohta, H., Wenk, M.R. and Ito, T. (2014) Transcriptomic and lipidomic profiles of glycerolipids during A rabidopsis flower development. New Phytol. 203, 310-322.
Näsholm, T., Kielland, K. and Ganeteg, U. (2009) Uptake of organic nitrogen by plants. New Phytol. 182, 31-48.
Nepi, M. and Stpiczynska, M. (2008) Do plants dynamically regulate nectar features through sugar sensing? Plant Signal. Behav. 3, 874-876.
Ngugi, H.K. and Scherm, H. (2006) Biology of flower-infecting fungi. Annu. Rev. Phytopathol. 44, 261-282.
Noctor, G. and Mhamdi, A. (2017) Climate change, CO2, and defense: the metabolic, redox, and signaling perspectives. Trends Plant Sci. 22, 857-870.
Pedersen, M.W., Lefevre, C.W. and Wiebe, H.H. (1958) Absorption of C14-labeled sucrose by alfalfa nectaries. Science (New York, N.Y.), 127, 758-759.
Polturak, G. and Aharoni, A. (2018) "La Vie en Rose": biosynthesis, sources, and applications of betalain pigments. Mol. Plant, 11, 7-22.
Prado, S.G., Collazo, J.A., Stevenson, P.C. and Irwin, R.E. (2019) A comparison of coffee floral traits under two different agricultural practices. Sci. Rep. 9, 1-13.
Prasifka, J.R., Mallinger, R.E., Portlas, Z.M., Hulke, B.S., Fugate, K.K., Paradis, T., Hampton, M.E. and Carter, C.J. (2018) Using nectar-related traits to enhance crop-pollinator interactions. Front. Plant Sci. 9, 812.
Rocha, O., Ansari, K. and Doohan, F. (2005) Effects of trichothecene mycotoxins on eukaryotic cells: a review. Food Addit. Contam. 22, 369-378.
Rottmann, T., Fritz, C., Sauer, N. and Stadler, R. (2018) Glucose uptake via STP transporters inhibits in vitro pollen tube growth in a HEXOKINASE1-dependent manner in Arabidopsis thaliana. Plant Cell, 30, 2057-2081.
Roulston, T.H., Cane, J.H. and Buchmann, S.L. (2000) What governs protein content of pollen: pollinator preferences, pollen-pistil interactions, or phylogeny? Ecol. Monogr. 70, 617-643.
Roy, R., Schmitt, A.J., Thomas, J.B. and Carter, C.J. (2017) Nectar biology: from molecules to ecosystems. Plant Sci. 262, 148-164.
Ruan, Y.-L., Patrick, J.W., Bouzayen, M., Osorio, S. and Fernie, A.R. (2012) Molecular regulation of seed and fruit set. Trends Plant Sci. 17, 656-665.
Ruhlmann, J.M., Kram, B.W. and Carter, C.J. (2010) CELL WALL INVERTASE 4 is required for nectar production in Arabidopsis. J. Exp. Bot. 61, 395-404.
Schmitt, A.J., Roy, R., Klinkenberg, P.M., Jia, M. and Carter, C.J. (2018) The octadecanoid pathway, but not COI1, is required for nectar secretion in Arabidopsis thaliana. Front. Plant Sci. 9, 1060.
Schnepp, J. and Dudareva, N. (2018) Floral scent: biosynthesis, regulation and genetic modifications. Ann. Plant Rev. Online, 240-257.
Schwachtje, J., Whitcomb, S.J., Firmino, A.A.P., Zuther, E., Hincha, D.K. and Kopka, J. (2019) Induced, imprinted, and primed responses to changing environments: does metabolism store and process information? Front. Plant Sci. 10, 106.
Seifi, H.S., Van Bockhaven, J., Angenon, G. and Hofte, M. (2013) Glutamate metabolism in plant disease and defense: friend or foe? Mol. Plant Microbe Interact. 26, 475-485.
Shahri, W. and Tahir, I. (2014) Flower senescence: some molecular aspects. Planta, 239, 277-297.
Shan, H., Cheng, J., Zhang, R., Yao, X. and Kong, H. (2019) Developmental mechanisms involved in the diversification of flowers. Nat. Plants, 5, 917-923.
Shibuya, K., Niki, T. and Ichimura, K. (2013) Pollination induces autophagy in petunia petals via ethylene. J. Exp. Bot. 64, 1111-1120.
Smith, M., Saks, Y. and Staden, J.v. (1992) Ultrastructural changes in the petals of senescing flowers of Dianthus caryophyllus L. Ann. Bot. 69, 277-285.
Solhaug, E.M., Johnson, E. and Carter, C.J. (2019a) Carbohydrate metabolism and signaling in squash nectaries and nectar throughout floral maturation. Plant Physiol. 180, 1930-1946.
Solhaug, E.M., Roy, R., Chatt, E.C., Klinkenberg, P.M., Mohd-Fadzil, N.A., Hampton, M., Nikolau, B.J. and Carter, C.J. (2019b) An integrated transcriptomics and metabolomics analysis of the Cucurbita pepo nectary implicates key modules of primary metabolism involved in nectar synthesis and secretion. Plant Direct, 3, e00120.
Sosso, D., Van Der Linde, K., Bezrutczyk, M., Schuler, D., Schneider, K., Kämper, J. and Walbot, V. (2019) Sugar partitioning between Ustilago maydis and its host Zea mays L during infection. Plant Physiol. 179, 1373-1385.
Southwick, E. (1984) Photosynthate allocation to floral nectar: a neglected energy investment. Ecology, 65, 1775-1779.
Specht, C.D. and Howarth, D.G. (2015) Adaptation in flower form: a comparative evodevo approach. New Phytol. 206, 74-90.
Stanley, L.E., Ding, B., Sun, W., Mou, F.-J., Hill, C., Chen, S. and Yuan, Y.-W. (2020) A tetratricopeptide repeat protein regulates carotenoid biosynthesis and chromoplast development in monkeyflower (Mimulus). The Plant Cell. 32, 1536-1555.
Stead, A. (1992) Pollination-induced flower senescence: a review. Plant Growth Regul. 11, 13-20.
Steiner, B., Buerstmayr, M., Wagner, C., Danler, A., Eshonkulov, B., Ehn, M. and Buerstmayr, H. (2019) Fine-mapping of the Fusarium head blight resistance QTL Qfhs.ifa-5A identifies two resistance QTL associated with anther extrusion. Theor. Appl. Genet. 132, 2039-2053.
Stevenson, P.C. (2019) For antagonists and mutualists: the paradox of insect toxic secondary metabolites in nectar and pollen. Phytochem. Rev. 1-12.
Stitz, M., Hartl, M., Baldwin, I.T. and Gaquerel, E. (2014) Jasmonoyl-L-isoleucine coordinates metabolic networks required for anthesis and floral attractant emission in wild tobacco (Nicotiana attenuata). Plant Cell, 26, 3964-3983.
Tanaka, S., Brefort, T., Neidig, N., Djamei, A., Kahnt, J., Vermerris, W., Koenig, S., Feussner, K., Feussner, I. and Kahmann, R. (2014) A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. eLife, 3, e01355.
Tegeder, M. (2012) Transporters for amino acids in plant cells: some functions and many unknowns. Curr. Opin. Plant Biol. 15, 315-321.
Tegeder, M. and Hammes, U.Z. (2018) The way out and in: phloem loading and unloading of amino acids. Current Opin. Plant Biol. 43, 16-21.
Terry, M.I., Pérez-Sanz, F., Díaz-Galián, M., Pérez de los Cobos, F., Navarro, P.J., Egea-Cortines, M. and Weiss, J. (2019) The Petunia CHANEL gene is a ZEITLUPE ortholog coordinating growth and scent profiles. Cells, 8, 343.
Theis, N. and Adler, L.S. (2012) Advertising to the enemy: enhanced floral fragrance increases beetle attraction and reduces plant reproduction. Ecology, 93, 430-435.
Thomson, B. and Wellmer, F. (2019) Molecular regulation of flower development. Current Topics in Developmental Biology (Grossniklaus, U., ed). Cambridge, MA: Academic Press (Elsevier), pp. 185-210.
Vaknin, H., Bar-Akiva, A., Ovadia, R., Nissim-Levi, A., Forer, I., Weiss, D. and Oren-Shamir, M. (2005) Active anthocyanin degradation in Brunfelsia calycina (yesterday-today-tomorrow) flowers. Planta, 222, 19-26.
van der Sluijs, J.P. and Vaage, N.S. (2016) Pollinators and global food security: the need for holistic global stewardship. Food ethics, 1, 75-91.
van Doorn, W.G. and Woltering, E.J. (2008) Physiology and molecular biology of petal senescence. J. Exp. Bot. 59, 453-480.
Verdonk, J.C., Haring, M.A., van Tunen, A.J. and Schuurink, R.C. (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell, 17, 1612-1624.
Walter, S., Nicholson, P. and Doohan, F.M. (2010) Action and reaction of host and pathogen during Fusarium head blight disease. New Phytol. 185, 54-66.
Wang, P., Liao, H., Zhang, W., Yu, X., Zhang, R., Shan, H., Duan, X., Yao, X. and Kong, H. (2015) Flexibility in the structure of spiral flowers and its underlying mechanisms. Nat. Plants, 2, 1-10.
Widhalm, J.R., Gutensohn, M., Yoo, H., Adebesin, F., Qian, Y., Guo, L., Jaini, R., Lynch, J.H., McCoy, R.M. and Shreve, J.T. (2015) Identification of a plastidial phenylalanine exporter that influences flux distribution through the phenylalanine biosynthetic network. Nat. Commun. 6, 1-11.
Wils, C.R. and Kaufmann, K. (2017) Gene-regulatory networks controlling inflorescence and flower development in Arabidopsis thaliana. Biochimica et Biophysica Acta (BBA) - Gene Regul. Mech. 1860, 95-105.
Wotton, K.R., Gao, B., Menz, M.H., Morris, R.K., Ball, S.G., Lim, K.S., Reynolds, D.R., Hu, G. and Chapman, J.W. (2019) Mass seasonal migrations of hoverflies provide extensive pollination and crop protection services. Curr. Biol. 29, 2167-2173.e5
Xu, W., Dubos, C. and Lepiniec, L. (2015) Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci. 20, 176-185.
Xu, Y. and Hanson, M.R. (2000) Programmed cell death during pollination-induced petal senescence in petunia. Plant Physiol. 122, 1323-1334.
Yuan, L., Graff, L., Loqué, D., Kojima, S., Tsuchiya, Y.N., Takahashi, H. and von Wirén, N. (2009) AtAMT1; 4, a pollen-specific high-affinity ammonium transporter of the plasma membrane in Arabidopsis. Plant Cell Physiol. 50, 13-25.
Zhang, J., Huang, Q., Zhong, S., Bleckmann, A., Huang, J., Guo, X., Lin, Q., Gu, H., Dong, J. and Dresselhaus, T. (2017) Sperm cells are passive cargo of the pollen tube in plant fertilization. Nat. Plants, 3, 17079.
Zhang, J.Z., Laudencia-Chingcuanco, D.L., Comai, L., Li, M. and Harada, J.J. (1994) Isocitrate lyase and malate synthase genes from Brassica napus L. are active in pollen. Plant Physiol. 104, 857-864.
Zhang, X.-W., Jia, L.-J., Zhang, Y., Jiang, G., Li, X., Zhang, D. and Tang, W.-H. (2012) In planta stage-specific fungal gene profiling elucidates the molecular strategies of Fusarium graminearum growing inside wheat coleoptiles. Plant Cell, 24, 5159-5176.
Zhong, S., Liu, M., Wang, Z., Huang, Q., Hou, S., Xu, Y.-C., Ge, Z., Song, Z., Huang, J. and Qiu, X. (2019) Cysteine-rich peptides promote interspecific genetic isolation in Arabidopsis. Science (New York, N.Y.), 364, eaau9564.
Zhou, L.-Z. and Dresselhaus, T. (2019) Friend or foe: signaling mechanisms during double fertilization in flowering seed plants. In Current Topics in Developmental Biology (Grossniklaus, U., ed). Cambridge, MA: Academic Press (Elsevier), pp. 453-496.