New Insights into the Early Steps of Oil Body Mobilization During Pollen Germination

Overview

Journal J Exp Bot

Publisher Oxford University Press

Specialty Biology

Date 2012 Nov 8

PMID 23132905

Citations 17

Authors

Agnieszka Zienkiewicz

Krzysztof Zienkiewicz

Juan David Rejon

Maria Isabel Rodriguez-Garcia

Antonio Jesus Castro

Affiliations

Soon will be listed here.

Abstract

In some plants, pollen grains accumulate storage lipids that serve as energy supply during germination. Here, three enzymes involved in early steps of oil body mobilization in the male gametophyte were functionally characterized for the first time. The effect of extracellular sugars on pollen performance and oil body dynamics was also analysed. Olive pollen oil bodies showed phospholipase A, lipase, and lipoxygenase activities on their surface. Enzyme activity levels increased during germination with a maximum after 3h. Removal of extracellular sugars from the germination medium did not affect pollen performance but increased enzyme activity rates and sped up oil body mobilization. Inhibitors seriously hampered pollen germination and pollen tube growth, leading to a characteristic accumulation of oil bodies in the germinative aperture. It can be concluded that storage lipids are sufficient for proper olive pollen germination. A lipase and a lipoxygenase are likely involved in oil body mobilization. Extracellular sugars may modulate their function, while a phospholipase A may promote their access to the storage lipids.

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References

Zienkiewicz K, Zienkiewicz A, Rodriguez-Garcia M, Castro A . Characterization of a caleosin expressed during olive (Olea europaea L.) pollen ontogeny. BMC Plant Biol. 2011; 11:122. PMC: 3180362. DOI: 10.1186/1471-2229-11-122. View

Graham I . Seed storage oil mobilization. Annu Rev Plant Biol. 2008; 59:115-42. DOI: 10.1146/annurev.arplant.59.032607.092938. View

Borek S, Nuc K . Sucrose controls storage lipid breakdown on gene expression level in germinating yellow lupine (Lupinus luteus L.) seeds. J Plant Physiol. 2011; 168(15):1795-803. DOI: 10.1016/j.jplph.2011.05.016. View

Matsui K, Hijiya K, Tabuchi Y, Kajiwara T . Cucumber cotyledon lipoxygenase during postgerminative growth. Its expression and action on lipid bodies. Plant Physiol. 1999; 119(4):1279-88. PMC: 32012. DOI: 10.1104/pp.119.4.1279. View

El-Kouhen K, Blangy S, Ortiz E, Gardies A, Ferte N, Arondel V . Identification and characterization of a triacylglycerol lipase in Arabidopsis homologous to mammalian acid lipases. FEBS Lett. 2005; 579(27):6067-73. DOI: 10.1016/j.febslet.2005.09.072. View

Matsui K, Fukutomi S, Ishii M, Kajiwara T . A tomato lipase homologous to DAD1 (LeLID1) is induced in post-germinative growing stage and encodes a triacylglycerol lipase. FEBS Lett. 2004; 569(1-3):195-200. DOI: 10.1016/j.febslet.2004.05.064. View

Shakya R, Bhatla S . A comparative analysis of the distribution and composition of lipidic constituents and associated enzymes in pollen and stigma of sunflower. Sex Plant Reprod. 2010; 23(2):163-72. DOI: 10.1007/s00497-009-0125-0. View

Maccarrone M, Salucci M, van Zadelhoff G, Malatesta F, Veldink G, Vliegenthart J . Tryptic digestion of soybean lipoxygenase-1 generates a 60 kDa fragment with improved activity and membrane binding ability. Biochemistry. 2001; 40(23):6819-27. DOI: 10.1021/bi010187m. View

Hills M, Murphy D, Beevers H . Inhibition of Neutral Lipase from Castor Bean Lipid Bodies by Coenzyme A (CoA) and Oleoyl-CoA. Plant Physiol. 1989; 89(3):1006-10. PMC: 1055958. DOI: 10.1104/pp.89.3.1006. View

10.

Murphy D . The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma. 2011; 249(3):541-85. DOI: 10.1007/s00709-011-0329-7. View

11.

Zienkiewicz K, Castro A, de Dios Alche J, Zienkiewicz A, Suarez C, Rodriguez-Garcia M . Identification and localization of a caleosin in olive (Olea europaea L.) pollen during in vitro germination. J Exp Bot. 2010; 61(5):1537-46. PMC: 2837266. DOI: 10.1093/jxb/erq022. View

12.

Bago B, Zipfel W, Williams R, Jun J, Arreola R, Lammers P . Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol. 2002; 128(1):108-24. PMC: 148950. View

13.

Andreou A, Feussner I . Lipoxygenases - Structure and reaction mechanism. Phytochemistry. 2009; 70(13-14):1504-10. DOI: 10.1016/j.phytochem.2009.05.008. View

14.

Rodriguez-Garcia M, Mrani-Alaoui M, Fernandez M . Behavior of storage lipids during development and germination of olive ( Olea europaea L.) pollen. Protoplasma. 2003; 221(3-4):237-44. DOI: 10.1007/s00709-002-0076-x. View

15.

Yadav M, Bhatla S . Localization of lipoxygenase activity on the oil bodies and in protoplasts using a novel fluorescence imaging method. Plant Physiol Biochem. 2010; 49(2):230-4. DOI: 10.1016/j.plaphy.2010.11.012. View

16.

Suarez C, Castro A, Rapoport H, Rodriguez-Garcia M . Morphological, histological and ultrastructural changes in the olive pistil during flowering. Sex Plant Reprod. 2012; 25(2):133-46. DOI: 10.1007/s00497-012-0186-3. View

17.

Wolters-Arts M, Lush W, Mariani C . Lipids are required for directional pollen-tube growth. Nature. 1998; 392(6678):818-21. DOI: 10.1038/33929. View

18.

Mayfield J, Fiebig A, Johnstone S, Preuss D . Gene families from the Arabidopsis thaliana pollen coat proteome. Science. 2001; 292(5526):2482-5. DOI: 10.1126/science.1060972. View

19.

Hanano A, Burcklen M, Flenet M, Ivancich A, Louwagie M, Garin J . Plant seed peroxygenase is an original heme-oxygenase with an EF-hand calcium binding motif. J Biol Chem. 2006; 281(44):33140-51. DOI: 10.1074/jbc.M605395200. View

20.

Feussner I, Wasternack C, Kindl H, Kuhn H . Lipoxygenase-catalyzed oxygenation of storage lipids is implicated in lipid mobilization during germination. Proc Natl Acad Sci U S A. 1995; 92(25):11849-53. PMC: 40500. DOI: 10.1073/pnas.92.25.11849. View