Deficiency in a Very-Long-Chain Fatty Acid β-Ketoacyl-Coenzyme A Synthase of Tomato Impairs Microgametogenesis and Causes Floral Organ Fusion

• Published in: Plant physiology (Bethesda) Vol. 161; no. 1; pp. 196 - 209
• Main Authors: Smirnova, Anna, Leide, Jana, Riederer, Markus
• Format: Journal Article
• Language: English
• Published: Rockville, MD American Society of Plant Biologists 01.01.2013
• Subjects: 3-Oxoacyl-(Acyl-Carrier-Protein) Synthase - genetics; 3-Oxoacyl-(Acyl-Carrier-Protein) Synthase - metabolism; alkanes; Anthers; Arabidopsis thaliana; Biological and medical sciences; Biology and morphogenesis of the reproductive apparatus. Photoperiodism, vernalisation; Biosynthesis; Cell Membrane - genetics; Cell Membrane - metabolism; Cell Membrane - physiology; Cell Wall - genetics; Cell Wall - metabolism; Cell Wall - physiology; cross pollination; cutin; Cytoplasm - genetics; Cytoplasm - metabolism; epicuticular wax; Epidermal cells; Flower buds; Flowering; flowers; Flowers - enzymology; Flowers - physiology; Flowers - ultrastructure; fruits; Fundamental and applied biological sciences. Psychology; Gametogenesis, Plant; Gene Expression Regulation, Plant; GENES, DEVELOPMENT, AND EVOLUTION; Genes, Plant; Germ Cells, Plant - metabolism; Germ Cells, Plant - physiology; Germ Cells, Plant - ultrastructure; leaves; Lycopersicon esculentum - anatomy & histology; Lycopersicon esculentum - enzymology; Lycopersicon esculentum - genetics; Lycopersicon esculentum - physiology; male fertility; Membrane Lipids - metabolism; Microscopy, Electron, Scanning; Microscopy, Electron, Transmission; Microspores; mutants; mutation; Petals; Phenotype; Plant Epidermis - metabolism; Plant Epidermis - ultrastructure; Plant Infertility; Plant physiology and development; Plant Proteins - genetics; Plant Proteins - metabolism; Plants; Pollen; pollen flow; Pollination; Reproduction; sexual reproduction; Solanum lycopersicum; Species Specificity; Substrate Specificity; tomatoes; Transcription, Genetic; ultrastructure; Vegetative and sexual reproduction, floral biology, fructification; very long chain fatty acids; Waxes; Waxes - metabolism; Flower; Enzyme; Long chain; Synthase; Tomato; Fatty acids; Vegetable crop; Plant physiology; Dicotyledones; Angiospermae; Lycopersicon esculentum; Coenzyme A; Spermatophyta; Solanaceae; Plant reproductive apparatus
• ISSN: 0032-0889; 1532-2548; 1532-2548
• DOI: 10.1104/pp.112.206656

Previously, it was shown that β-ketoacyl-coenzyme A synthase ECERIFERUM6 (CER6) is necessary for the biosynthesis of verylong-chain fatty acids with chain lengths beyond C₂₈ in tomato (Solanum lycopersicum) fruits and C₂₆ in Arabidopsis (Arabidopsis thaliana) leaves and the pollen coat. CER6 loss of function in Arabidopsis resulted in conditional male sterility, since pollen coat lipids are responsible for contact-mediated pollen hydration. In tomato, on the contrary, pollen hydration does not rely on pollen coat lipids. Nevertheless, mutation in SlCER6 impairs fertility and floral morphology. Here, the contribution of SlCER6 to the sexual reproduction and flower development of tomato was addressed. Cytological analysis and cross-pollination experiments revealed that the slcer6 mutant has male sterility caused by (1) hampered pollen dispersal and (2) abnormal tapetum development. SICER6 loss of function provokes a decrease of n-and zso-alkanes with chain lengths of C₂₇ or greater and of anteiso-alkanes with chain lengths of C₂₈ or greater in flower cuticular waxes, but it has no impact on flower cuticle ultrastructure and cutin content. Expression analysis confirmed high transcription levels of SlCER6 in the anther and the petal, preferentially in sites subject to epidermal fusion. Hence, wax deficiency was proposed to be the primary reason for the flower fusion phenomenon in tomato. The SlCER6 substrate specificity was revisited. It might be involved in elongation of not only linear but also branched very-long-chain fatty acids, leading to production of the corresponding alkanes. SlCER6 implements a function in the sexual reproduction of tomato that is different from the one in Arabidopsis: SlCER6 is essential for the regulation of timely tapetum degradation and, consequently, microgametogenesis.