Abstract
Main conclusion
The close association between membranes and organelles, and the intense chloroplast remodeling in parenchyma cells of extrafloral nectaries occurred only at the secretion time and suggest a relationship with the nectar secretion.
Associations between membranes and organelles have been well documented in different tissues and cells of plants, but poorly explored in secretory cells. Here, we described the close physical juxtaposition between membranes and organelles, mainly with chloroplasts, in parenchyma cells of Citharexylum myrianthum (Verbenaeceae) extrafloral nectaries under transmission electron microscopy, using conventional and microwave fixation. At the time of nectar secretion, nectary parenchyma cells exhibit a multitude of different organelle and membrane associations as mitochondria–mitochondria, mitochondria–endoplasmic reticulum, mitochondria–chloroplast, chloroplast–nuclear envelope, mitochondria–nuclear envelope, chloroplast–plasmalemma, chloroplast–chloroplast, chloroplast–tonoplast, chloroplast–peroxisome, and mitochondria–peroxisome. These associations were visualized as amorphous electron-dense material, a network of dense fibrillar material and/or dense bridges. Chloroplasts exhibited protrusions variable in shape and extension, which bring them closer to each other and to plasmalemma, tonoplast, and nuclear envelope. Parenchyma cells in the pre- and post-secretory stages did not exhibit any association or juxtaposition of membranes and organelles, and chloroplast protrusions were absent. Chloroplasts had peripheral reticulum that was more developed in the secretory stage. We propose that such subcellular phenomena during the time of nectar secretion optimize the movement of signaling molecules and the exchange of metabolites. Our results open new avenues on the potential mechanisms of organelle contact in parenchyma nectary cells, and reveal new attributes of the secretory cells on the subcellular level.
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Abbreviations
- EFN:
-
Extrafloral nectaries
- ER:
-
Endoplasmic reticulum
- RER:
-
Rough endoplasmic reticulum
- PR:
-
Peripheral reticulum
- CPs:
-
Chloroplast protrusions
References
Benayoun J, Fahn A (1979) Intracellular transport and elimination of resin from epithelial duct-cells of Pinus halepensis. Ann Bot 43:179–181
Bosabalidis A, Tsekos I (1982) Ultrastructural studies on the secretory cavities of Citrus deliciosa Ten. II. Development of the oil-accumulating central space of the gland and process of active secretion. Protoplasma 112:63–70
Bracker CE, Grove SN (1971) Continuity between cytoplasmic endomembranes and outer mitochondrial membranes in fungi. Protoplasma 73:15–34
Breuers FKH, Bräutigam A, Geimer S, Welzel U, Stefano G, Renna L, Brandizzi F, Weber APM (2012) Dynamic remodeling of the plastid envelope membranes—a tool for chloroplast envelope in vivo localizations. Front Plant Sci 3(7):10
Buchner O, Moser T, Karadar M, Roach T, Kranner I, Holzinger A (2015) Formation of chloroplast protrusions and catalase activity in alpine Ranunculus glacialis under elevated temperature and different CO2/O2 ratios. Protoplasma 252:1613–1619
Caplan JL, Kumar AS, Park E, Padmanabhan MS, Hoban K, Modla S, Czymmek K, Dinesh-Kumar SP (2015) Chloroplast stromules function during innate immunity. Dev Cell 34:45–57
Carothers ZB (1972) Studies of spermatogenesis in the hepatical. III. Continuity between plasma membrane and nuclear envelope in andragonial cells of Blasia. J Cell Biol 52:273–282
Cheniclet C, Carde JP (1985) Presence of leucoplasts in secretory cells and of monoterpenes in the essential oil: a correlative study. Isr J Bot 34:219–238
Cran DG, Dyer AF (1973) Membrane continuity and associations in the fern Dryopteris borreri. Protoplasma 76:103–108
Crotty WJ, Ledbetter MC (1973) Membrane continuities involving chloroplasts and other organelles in plant cells. Science 82:839–841
Delfosse K, Wozny MR, Jaipargas E-A, Barton KA, Anderson C, Mathur J (2016) Fluorescent protein aided insights on plastids and their extensions: a critical appraisal. Front Plant Sci 6:1253. https://doi.org/10.3389/fpls.2015.01253
Evert RF (2006) Esau’s plant anatomy: meristems, cells, and tissues of the plant body–their structure, function, and development, 3rd edn. John Wiley & Sons, Hoboken
Fahn A (1979) Secretory tissues in plants. Academic Press, London
Franke WW, Kartenbeck J (1971) Outer mitochondrial membrane continuous with endoplasmic reticulum. Protoplasma 73:35–41
Freeman TP, Duysen ME (1975) The effect of imposed water stress on the development and ultrastructure of wheat chloroplasts. Protoplasma 83:131–145
Gallo A, Vannier C, Galli T (2016) Endoplasmic reticulum-plasma membrane associations: structures and functions. Ann Rev Cell Dev Biol 32:279–301
Gracen VE Jr, Hilliard JH, Brown RH, West SH (1972) Peripheral reticulum in chloroplasts of plants differing in CO2 fixation pathways and photorespiration. Planta 107:189–204
Gray JC, Sullivan JA, Hibberd JM, Hanson MR (2001) Stromules: mobile protrusions and interconnections between plastids. Plant Biol 3:223–233
Griffing LR, Lin C, Perico C, White RR, Sparkes I (2017) Plant ER geometry and dynamics: biophysical and cytoskeletal control during growth and biotic response. Protoplasma 254:43–56
Guo J, Yuan Y, Liu Z, Zhu J (2013) Development and structure of internal glands and external glandular trichomes in Pogostemon cablin. PLoS One 8(10):e77862. https://doi.org/10.1371/journal.pone.0077862
Hanson MR, Sattarzadeh A (2008) Dynamic morphology of plastids and stromules in angiosperm plants. Plant Cell Environ 31:646–657
Hanson MR, Sattarzadeh A (2011) Stromules: recent insights into a long neglected feature of plastid morphology and function. Plant Physiol 155:1486–1492
Hanson MR, Sattarzadeh A (2013) Trafficking of proteins through plastid stromules. Plant Cell 25:2774–2782
Heldt HW, Saur F (1971) The inner membrane of the chloroplast envelope as a site of specific metabolite transport. Biochim Biophys Acta 243:83–91
Holzinger A, Buchner O, Lütz C, Hanson MR (2007a) Temperature sensitive formation of chloroplast protrusions and stromules in mesophyll cells of Arabidopsis thaliana. Protoplasma 230:23–30
Holzinger A, Wasteneys GO, Lütz C (2007b) Investigating cytoskeletal function in chloroplast protrusion formation in the Arctic-Alpine plant Oxyria digyna. Plant Biol 9:400–410
Kumar A, Dinesh-Kumar SP, Caplan J (2014) Stromules. In: Theg S, Wollman F (eds) Adv plant biol: plastid biology, vol 5. Springer, New York, pp 189–207
Kwok EY, Hanson MR (2003) Microfilaments and microtubules control the morphology and movement of non-green plastids and stromules in Nicotiana tabacum. Plant J 35:16–26
Kwok EY, Hanson MR (2004) Stromules and the dynamic nature of plastid morphology. J Microsc 214:124–137
Laetsch WM (1974) The C4 syndrome: a structural analysis. Ann Rev Plant Physiol 25:27–52
Lee HY, Bowen CH, Popescu GV, Kang HG, Kato N, Ma S, Dinesh-Kumar S, Snyder M, Popescu SC (2012) Arabidopsis RTNLB1 and RTNLB2 reticulon-like proteins regulate intracellular trafficking and activity of the FLS2 immune receptor. Plant Cell 23:3374–3391
Login GR, Stavinoha WB, Dvorak AM (1986) Ultrafast microwave energy fixation for electron microscopy. J Histochem Cytochem 34:381–387
Lütz C, Engel L (2007) Changes in chloroplast ultrastructure in some high-alpine plants: adaptation to metabolic demands and climate? Protoplasma 231:183–192
Maier K, Maier U (1968) Zur Frage einer Neubildung von mitochondrion aus plastiden. Protoplasma 65:239–242
McLean B, Whatley JM, Juniper BE (1988) Continuity of chloroplast and endoplasmic reticulum membranes in Chara and Equisetum. New Phytol 109:59–63
Mehrshahi P, Stefano G, Andaloro JM, Brandizzi F, Froehlich JE, DellaPenna D (2013) Transorganellar complementation redefines the biochemical continuity of endoplasmic reticulum and chloroplasts. PNAS 110:12126–12131. https://doi.org/10.1073/pnas.1306331110
Miyake H, Furukawa A, Totsuka T (1985) Structural associations between mitochondria and chloroplasts in the bundle sheath cells of Portulaca oleracea. Ann Bot 55:815–817
Montes G, Bradbeer U (1976) An association of chloroplasts and mitochondria in Zea mays and Hyptis suaveolena. Plant Sci Lett 6:35–41
Morré DJ, Merrit WD, Lembi CA (1971) Connections between mitochondria and endoplasmic reticulum in rat liver and onion stem. Protoplasma 73:43–49
Moser T, Holzinger A, Buchner O (2015) Chloroplast protrusions in leaves of Ranunculus glacialis L. respond significantly to different ambient conditions but are not related to temperature stress. Plant Cell Environ 38:1347–1356
Nepi M (2007) Nectary structure and ultrastructure. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Dordrecht, pp 129–166
Possobom CCF, Machado SR (2017) Elaiphores in three Neotropical Malpighiaceae species: a comparative study. Plant Syst Evol. https://doi.org/10.1007/s00606-017-1443-6
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
Robards AW, Stark M (1988) Nectar secretion in Abutilon: a new model. Protoplasma 142:79–91
Robertson EJ, Rutherford SM, Leech RM (1996) Characterization of chloroplast division using the Arabidopsis mutant arc5. Plant Physiol 112:149–159
Rodrigues TM, Teixeira SP, Machado SR (2011) The oleoresin secretory system in seedlings and adult plants of copaíba (Copaifera langsdorffii Desf., Leguminosae–Caesalpinioideae). Flora (Jena) 206:585–594
Schattat M, Barton K, Baudisch B, Klosgen RB, Mathur J (2011) Plastid stromule branching coincides with contiguous endoplasmic reticulum dynamics. Plant Physiol 155:1667–1677
Schattat MH, Barton KA, Mathur J (2015) The myth of interconnected plastids and related phenomena. Protoplasma 252:359–371
Szczepanik J, Sowiński P (2014) The occurrence of chloroplast peripheral reticulum in grasses: a matter of phylogeny or a matter of function? Acta Physiol Plant 36:1133–1142
Taiz L, Zeiger E (2013) Plant physiology, 5th edn. Sinauer Associates Inc. Publishers, Sunderland
Wang P, Hussey PJ (2015) Interactions between plant endomembrane systems and the actin cytoskeleton. Front Plant Sci 6:422
Whatley JM, McLean B, Juniper BE (1991) Continuity of chloroplast and endoplasmic reticulum membranes in Phaseolus vulgaris. New Phytol 117:209–217
Wise RR (2006) The diversity of plastid form and function. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, Dordrecht, pp 3–26
Wu Y, Whiteus C, Shan XuC, Hayworth KJ, Weinberg RJ, Hess HF, De Camilli P (2017) Contacts between the endoplasmic reticulum and other membranes in neurons. PNAS 114:E4859–E4867
Yamane K, Mitsuya S, Taniguchi M, Miyake H (2012) Salt-induced chloroplast protrusion is the process of exclusion of ribulose-1,5-bisphosphate carboxylase/oxygenase from chloroplasts into cytoplasm in leaves of rice. Plant Cell Environ 35:1663–1671
Acknowledgements
This work was supported by the ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico’—CNPq (Grant to S.R. Machado Proc. 02657/2011-8, and Edital MCT/CNPq Proc. 470649/2008-9). We thank the staff of the Electron Microscopy Center of the São Paulo State University (UNESP), Institute of Biosciences, Campus of Botucatu (IBB), for the assistance with sample preparation.
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Machado, S.R., Gregório, E.A. & Rodrigues, T.M. Structural associations between organelle membranes in nectary parenchyma cells. Planta 247, 1067–1076 (2018). https://doi.org/10.1007/s00425-018-2844-7
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DOI: https://doi.org/10.1007/s00425-018-2844-7