Abstract
Anther and pollen development is a highly conserved process in angiosperms, but while pollen formation in annual plants occurs in a few days, in temperate woody perennials, it requires several months. How anther and pollen development is framed in terms of seasonality plays a clear part in reproductive success. In this study, seasonal anther and pollen development is characterized in two sweet cherry cultivars over 2 years, paying special attention to the period of dormancy and unveiling the role of starch in this process. We evaluated starch content from the autumn until bud burst with the help of an image analysis system fitted to a light microscope. Microscope observations allowed the temporal relationship of pollen development to the phenological stages of flower and bud development to be determined. In both cultivars and years, anther and pollen development followed the same pattern. Development was halted by dormancy, when the anthers showed no morphological changes until several weeks after chilling fulfillment, until the milder temperatures reactivated development. After dormancy, starch was accumulated in the connective tissue until tracheary element differentiation. Quantification of starch in the connective tissue of anthers revealed its importance in supporting pollen meiosis and subsequent anther growth.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alcaraz ML, Hormaza JI, Rodrigo J (2013) Pistil starch reserves at anthesis correlate with final flower fate in avocado (Persea americana). PLOSOne 8:e78467. https://doi.org/10.1371/journal.pone.0078467
Barton DA, Cantrill LC, Law AMK et al (2014) Chilling to zero degrees disrupts pollen formation but not meiotic microtubule arrays in Triticum aestivum L. Plant Cell Environ 37:2781–2794. https://doi.org/10.1111/pce.12358
Brukhin V, Hernould M, Gonzalez N, Chevalier C (2003) Flower development schedule in tomato Lycopersicon esculentum cv. sweet cherry. Sex Plant Reprod 15:311–320. https://doi.org/10.1007/s00497-003-0167-7
Bubán T, Faust M (1995) New aspects of bud dormancy in apple trees. Acta Hortic (395):105–111
Carrizo García C, Nepi M, Pacini E (2017) It is a matter of timing: asynchrony during pollen development and its consequences on pollen performance in angiosperms—a review. Protoplasma 254:57–73. https://doi.org/10.1007/s00709-016-0950-6
Chow PS, Landhausser SM (2004) A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol 24:1129–1136. https://doi.org/10.1093/treephys/24.10.1129
Citadin I, Bassols MC, Gilberto F et al (2002) Meiosis stage as an indicator for peach endodormancy. Rev Bras Frutic 24:23–28
Clement C, Pacini E (2001) Anther plastids in angiosperms. Bot Rev 67:54–73
El-Ghazaly G, Grafström E (1995) Morphological and histochemical differentiation of the pollen wall of Betula pendula Roth. during dormancy up to anthesis. Protoplasma 187:88–102
Fadón E, Herrero M, Rodrigo J (2015) Flower development in sweet cherry framed in the BBCH scale. Sci Hortic (Amsterdam) 192:141–147. https://doi.org/10.1016/j.scienta.2015.05.027
Fadón E, Rodrigo J (2018) Unveiling winter dormancy through empirical experiments. Environ Exp Bot 152:28–36. https://doi.org/10.1016/j.envexpbot.2017.11.006
Fadón E, Herrero M, Rodrigo J (2018a) Dormant flower buds actively accumulate starch over winter in sweet cherry. Front Plant Sci 9. https://doi.org/10.3389/fpls.2018.00171
Fadón E, Rodrigo J, Herrero M (2018b) Is there a specific stage to rest? Morphological changes in flower primordia in relation to endodormancy in sweet cherry (Prunus avium L.). Trees 32 (6):1583–1594. https://doi.org/10.1007/s00468-018-1735-7
Felker FC, Robitaille HA, Hess FD (1983) Morphological and ultrastructural development and starch accumulation during chilling of sour cherry flower buds. Am J Bot 70:376–386
Frenguelli G, Ferranti F, Tedeschini E, Andreutti R (1997) Volume changes in the pollen grain of Corylus avellana L. (Corylaceae) during development. Grana 36:289–292. https://doi.org/10.1080/00173139709362619
Gotelli MM, Galati BG, Zarlavsky G, Medan D (2016) Pollen and microsporangium development in Hovenia dulcis (Rhamnaceae): a different type of tapetal cell ultrastructure. Protoplasma 253:1125–1133. https://doi.org/10.1007/s00709-015-0870-x
Hedhly A, Hormaza JI, Herrero M (2004) Effect of temperature on pollen tube kinetics and dynamics in sweet cherry, Prunus avium (Rosaceae). Am J Bot 91:558–564. https://doi.org/10.3732/ajb.91.4.558
Hedhly A, Vogler H, Schmid MW, Pazmino D, Gagliardini V, Santelia D, Grossniklaus U (2016) Starch turnover and metabolism during flower and early embryo development. Plant Physiol 00916(2016):2388–2402. https://doi.org/10.1104/pp.16.00916
Herrero M, Rodrigo J, Wunsch A (2017) Flowering, fruit set and development. In: Quero-Garcia J, Iezzoni A, Lang G, Pulawska J (eds) Cherries: botany, production and uses. CAB International, Boston, pp 14–35
Iglesias DJ, Tadeo FR, Primo-Millo E, Talon M (2003) Fruit set dependence on carbohydrate availability in citrus trees. Tree Physiol 23:199–204. https://doi.org/10.1093/treephys/23.3.199
Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458. https://doi.org/10.1146/annurev.arplant.58.032806.103956
Julian C, Herrero M, Rodrigo J (2014) Anther meiosis time is related to winter cold temperatures in apricot (Prunus armeniaca L.). Environ Exp Bot 100:20–25. https://doi.org/10.1016/j.envexpbot.2013.12.002
Julian C, Rodrigo J, Herrero M (2011) Stamen development and winter dormancy in apricot (Prunus armeniaca). Ann Bot 108:617–625. https://doi.org/10.1093/aob/mcr056
Kim Y-J, Jang M-G, Zhu L, Silva J, Zhu X, Sukweenadhi J, Kwon WS, Yang DC, Zhang D (2016) Cytological characterization of anther development in Panax ginseng Meyer. Protoplasma 253:111–1124. https://doi.org/10.1007/s00709-015-0869-3
Koltunow AM, Truettner J, Cox KH, Wallroth M, Goldberg RB (1990) Different temporal and spatial gene expression patterns occur during anther development. Plant Cell 2:1201–1224. https://doi.org/10.1105/tpc.2.12.1201
Konyar S (2013) Ultrastructure of microsporogenesis and microgametogenesis in Campsis radicans (L.) Seem. (Bignoniaceae). Plant Syst Evol 300:303–320. https://doi.org/10.1007/s00606-013-0883-x
Kurokura T, Mimida N, Battey NH, Hytönen T (2013) The regulation of seasonal flowering in the Rosaceae. J Exp Bot 64:4131–4141. https://doi.org/10.1093/jxb/ert233
Lang GA, Early JD, Martin GC, Darnell RL (1987) Endodormancy, paradormancy, and ecodormancy—physiological terminology and classification for dormancy research. HortScience 22:371–377
Lebon G, Duchene E, Brun O et al (2004) Flower abscission and inflorescence carbohydrates in sensitive and non-sensitive cultivars of grapevine. Sex Plant Reprod 17:71–79. https://doi.org/10.1007/s00497-004-0217-9
Loescher WH, McCamant T, Keller JD (1990) Carbohydrate reserves, translocation and storage in woody plant roots. HortScience 25:274–281
Lora J, Herrero M, Hormaza J (2009a) The coexistence of bicellular and tricellular pollen in Annona cherimola (Annonaceae): implications for pollen evolution. Am J Bot 96:802–808. https://doi.org/10.3732/ajb.0800167
Lora J, Testillano PS, Risueño MC, Hormaza JI, Herrero M (2009b) Pollen development in Annona cherimola Mill. (Annonaceae). Implications for the evolution of aggregated pollen. BMC Plant Biol 9:129. https://doi.org/10.1186/1471-2229-9-129
Luza JG, Polito VS (1988) Microsporogenesis and anther differentiation in Juglans regia L.: a developmental basis for heterocichogamy in walnut. Bot Gaz 149:30–36
Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434. https://doi.org/10.1146/annurev.arplant.55.031903.141717
Mamun EA, Alfred S, Cantrill LC et al (2006) Effects of chilling on male gametophyte development in rice. Cell Biol Int 30:583–591. https://doi.org/10.1016/j.cellbi.2006.03.004
Mirgorodskaya OE, Koteyeva NK, Volchanskaya AV, Miroslavov EA (2015) Pollen development in Rhododendron in relation to winter dormancy and bloom time. Protoplasma 252:1313–1323. https://doi.org/10.1007/s00709-015-0764-y
Ohnishi S, Miyoshi T, Shirai S (2010) Low temperature stress at different flower developmental stages affects pollen development, pollination, and pod set in soybean. Environ Exp Bot 69:56–62. https://doi.org/10.1016/j.envexpbot.2010.02.007
Owen HA, Makaroff CA (1995) Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185:7–21
Pacini E (2010) Relationships between tapetum, loculus, and pollen during development. Int J Plant Sci 171:1–11. https://doi.org/10.1086/647923
Pacini E, Bellani LM, Lozzi R (1986) Pollen, tapetum and anther development in two cultivars of sweet cherry (Prunus avium). Phytomorphology 36:197–210
Pacini E, Dolferus R (2016) The trials and tribulations of the plant male gametophyte—understanding reproductive stage stress tolerance. In: Shanker A, Shanker C (eds) Abiotic and biotic stress in plants - recent advances and future perspectives. IntechOpen, pp 704–754
Pacini E, Jacquard C, Clément C (2011) Pollen vacuoles and their significance. Planta 234:217–227. https://doi.org/10.1007/s00425-011-1462-4
Reale L, Sgromo C, Ederli L, Pasqualini S, Orlandi F, Fornaciari M, Ferranti F, Romano B (2009) Morphological and cytological development and starch accumulation in hermaphrodite and staminate flowers of olive (Olea europaea L.). Sex Plant Reprod 22:109–119. https://doi.org/10.1007/s00497-009-0096-1
Richardson EA, Seeley SD, Walker DR (1974) A model for estimating the completion of rest for “Redhaven” and “Elberta” peach trees. HortScience 9:331–332
Richardson EA, Seeley SD, Walker DR et al (1975) Pheno-climatography of spring peach bud development. HortScience 10:236–237
Rodrigo J, Herrero M (1998) Influence of intraovular reserves on ovule fate in apricot (Prunus armeniaca L.). Sex Plant Reprod 11:86–93. https://doi.org/10.1007/s004970050124
Rodrigo J, Herrero M, Hormaza JI (2009) Pistil traits and flower fate in apricot (Prunus armeniaca). Ann Appl Biol 154:365–375. https://doi.org/10.1111/j.1744-7348.2008.00305.x
Rodrigo J, Hormaza JI, Herrero M (2000) Ovary starch reserves and flower development in apricot (Prunus armeniaca). Physiol Plant 108:35–41. https://doi.org/10.1034/j.1399-3054.2000.108001035.x
Rodrigo J, Rivas E, Herrero M (1997) Starch determination in plant tissues using a computerized image analysis system. Physiol Plant 99:105–110
Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12:217–223. https://doi.org/10.1016/j.tplants.2007.03.012
Ruiz R, García-Luis A, Monerry C, Guardiola JL (2001) Carbohydrate availability in relation to fruitlet abscission in Citrus. Ann Bot 87:805–812. https://doi.org/10.1006/anbo.2001.1415
Saito T, Tuan PA, Katsumi-Horigane A, Bai S, Ito A, Sekiyama Y, Ono H, Moriguchi T (2015) Development of flower buds in the Japanese pear (Pyrus pyrifolia) from late autumn to early spring. Tree Physiol 35:653–662. https://doi.org/10.1093/treephys/tpv043
Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767. https://doi.org/10.1105/tpc.2.8.755
Thalmann M, Santelia D (2017) Starch as a determinant of plant fitness under abiotic stress. New Phytol 214:943–951. https://doi.org/10.1111/nph.14491
Vogler H, Grossniklaus U, Hedhly A (2017) An introduction to male germline development. In: Schmidt A (ed) Plant germline development: methods and protocols. Humana Press Inc., Totowa, pp 3–15. https://doi.org/10.1007/978-1-4939-7286-9
Williams JH (2012a) Pollen tube growth rates and the diversification of flowering plant reproductive cycles. Int J Plant Sci 173:649–661. https://doi.org/10.1086/665822
Williams JH (2012b) The evolution of pollen germination timing in flowering plants: Austrobaileya scandens (Austrobaileyaceae). AoB Plants 12:1–12. https://doi.org/10.1093/aobpla/pls010
Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234. https://doi.org/10.1146/annurev-arplant-042809-112301
Zini LM, Galati BG, Zarlavsky G, Ferrucci MS (2017) Developmental and ultrastructural characters of the pollen grains and tapetum in species of Nymphaea subgenus Hydrocallis. Protoplasma 254:1–14. https://doi.org/10.1007/s00709-016-1074-8
Funding
This work was supported by the Ministerio de Ciencia, Innovación y Universidades—European Regional Development Fund, European Union: Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria [grant numbers RFP2015-00015-00, RTA2014-00085-00, RTA2017-00003-00] and Gobierno de Aragón—European Social Fund, European Union [Grupos Consolidados A43, A12_17R].
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Benedikt Kost
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Fadón, E., Herrero, M. & Rodrigo, J. Anther and pollen development in sweet cherry (Prunus avium L.) in relation to winter dormancy. Protoplasma 256, 733–744 (2019). https://doi.org/10.1007/s00709-018-01332-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-018-01332-4