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Pollen performance, cell number, and physiological state in the early-divergent angiosperm Annona cherimola Mill. (Annonaceae) are related to environmental conditions during the final stages of pollen development

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Abstract

Pollen performance is an important determinant for fertilization success, but high variability in pollen behavior both between and within species occurs in different years and under varying environmental conditions. Annona cherimola, an early-divergent angiosperm, is a species that releases a variable ratio of bicellular and tricellular hydrated pollen at anther dehiscence depending on temperature. The presence of both bi- and tricellular types of pollen is an uncommon characteristic in angiosperms and makes Annona cherimola an interesting model to study the effect of varying environmental conditions on subsequent pollen performance during the final stages of pollen development. In this work, we study the influence of changes in temperature and humidity during the final stages of pollen development on subsequent pollen performance, evaluating pollen germination, presence of carbohydrates, number of nuclei, and water content. At 25 °C, which is the average field temperature during the flowering period of this species, pollen had a viability of 60–70 %, starch hydrolyzed just prior to shedding, and pollen mitosis II was taking place, resulting in a mixture of bi- and tricellular pollen. This activity may be related to the pollen retaining 70 % water content at shedding. Temperatures above 30 °C resulted in a decrease in pollen germination, whereas lower temperatures did not have a clear influence on pollen germination, although they did have a clear effect on starch hydrolysis. On the other hand, slightly higher dehydration accelerated mitosis II, whereas strong dehydration arrested starch hydrolysis and reduced pollen germination. These results show a significant influence of environmental conditions on myriad pollen characteristics during the final stages of pollen development modifying subsequent pollen behavior and contributing to our understanding of the variability observed in pollen tube performance.

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References

  • Aloni B, Peet M, Pharr M, Karni L (2001) The effect of high temperature and high atmospheric CO2 on carbohydrate changes in bell pepper (Capsicum annuum) pollen in relation to its germination. Physiol Plant 112:505–512

    Article  PubMed  CAS  Google Scholar 

  • Baker HG, Baker I (1979) Starch in angiosperm pollen grains and its evolutionary significance. Am J Bot 66:591–600

    Article  Google Scholar 

  • Barnabas B, Kovacs G (1997) Storage of pollen. In: Shivanna K, Sawhney V (eds) Pollen biotechnology for crop production and improvement. Cambridge University Press, New York, pp 293–314

    Chapter  Google Scholar 

  • Borg M, Brownfield L, Twell D (2009) Male gametophyte development: a molecular perspective. J Exp Bot 60:1465–1478

    Article  PubMed  CAS  Google Scholar 

  • Brewbaker JL (1967) Distribution and phylogenetic significance of binucleate and trinucleate pollen grains in angiosperms. Am J Bot 54:1069–1083

    Article  Google Scholar 

  • Carrizo García C, Guarnieri M, Pacini E (2010) Soluble carbohydrates content in tomato pollen and its variations along and between blooming periods. Sci Hortic 125:524–527

    Article  Google Scholar 

  • Castro AJ, Clement C (2007) Sucrose and starch catabolism in the anther of Lilium during its development: a comparative study among the anther wall, locular fluid and microspore/pollen fractions. Planta 225:1573–1582

    Article  PubMed  CAS  Google Scholar 

  • Chatrou LW, Rainer H, Mass PJM (2004) Annonaceae. In: Stevenson DW, Heald SV, Smith N, Mori SA, Henderson A (eds) Flowering plants of the Neotropics. Princeton University Press, New Jersey, pp 18–20

    Google Scholar 

  • Clement C, Pacini E (2001) Anther plastids in angiosperms. Bot Rev 67:54–73

    Article  Google Scholar 

  • Couvreur TLP, Pirie MD, Chatrou LW, Saunders RMK, Su YCF, Richardson JE, Erkens RHJ (2011) Early evolutionary history of the flowering plant family Annonaceae: steady diversification and boreotropical geodispersal. J Biogeogr 38:664–680

    Article  Google Scholar 

  • Delph LF, Johannsson MH, Stephenson AG (1997) How environmental factors affect pollen performance: ecological and evolutionary perspectives. Ecology 78:1632–1639

    Article  Google Scholar 

  • Demchik SM, Day TA (1996) Effect of enhanced UV-B radiation on pollen quantity, quality, and seed yield in Brassica rapa (Brassicaceae). Am J Bot 83:573–579

    Article  Google Scholar 

  • Endo M, Tsuchiya T, Hamada K, Kawamura S, Yano K, Ohshima M, Higashitani A, Watanabe M, Kawagishi-Kobayashi M (2009) High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development. Plant Cell Physiol 50:1911–1922

    Article  PubMed  CAS  Google Scholar 

  • Endress PK (2010) The evolution of floral biology in basal angiosperms. Philos Trans R Soc B 365:411–421

    Article  Google Scholar 

  • Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Am J Bot 55:123–142

    Article  Google Scholar 

  • Firon N, Shaked R, Peet MM, Pharr DM, Zamski E, Rosenfeld K, Althan L, Pressman E (2006) Pollen grains of heat tolerant tomato cultivars retain higher carbohydrate concentration under heat stress conditions. Sci Hortic 109:212–217

    Article  CAS  Google Scholar 

  • Franchi GG, Bellani L, Nepi M, Pacini E (1996) Types of carbohydrate reserves in pollen: Localization, systematic distribution and ecophysiological significance. Flora 191:143–159

    Google Scholar 

  • Franchi GG, Nepi M, Matthews ML, Pacini E (2007) Anther opening, pollen biology and stigma receptivity in the long blooming species, Parietaria judaica L. (Urticaceae). Flora 202:118–127

    Article  Google Scholar 

  • Friedman WE (1999) Expression of the cell cycle in sperm of Arabidopsis: implications for understanding patterns of gametogenesis and fertilization in plants and other eukaryotes. Development 126:1065–1075

    PubMed  CAS  Google Scholar 

  • Galen C, Stanton ML (2003) Sunny-side up: flower heliotropism as a source of parental environmental effects on pollen quality and performance in the snow buttercup, Ranunculus adoneus (Ranunculaceae). Am J Bot 90:724–729

    Article  PubMed  Google Scholar 

  • George AP, Nissen RJ, Ironside DA, Anderson P (1989) Effects of nitidulid beetles on pollination and fruit set of Annona spp. hybrids. Sci Hortic 39:289–299

    Article  Google Scholar 

  • Gottsberger G (1999) Pollination and evolution in neotropical Annonaceae. Plant Species Biol 14:143–152

    Article  Google Scholar 

  • Guarnieri M, Speranza A, Nepi M, Artese D, Pacini E (2006) Ripe pollen carbohydrate changes in Trachycarpus fortunei: the effect of relative humidity. Sex Plant Reprod 19:117–124

    Article  CAS  Google Scholar 

  • Havens K, Preston KA, Richardson C, Delph LF (1995) Nutrients affect allocation to male and female function in Abutilon theophrasti (Malvaceae). Am J Bot 82:726–733

    Article  Google Scholar 

  • Hedhly A (2011) Sensitivity of flowering plant gametophytes to temperature fluctuations. Environ Exp Bot 74:9–16

    Article  Google Scholar 

  • Hedhly A, Hormaza JI, Herrero M (2005) Influence of genotype–temperature interaction on pollen performance. J Evol Biol 18:1494–1502

    Article  PubMed  CAS  Google Scholar 

  • Hedhly A, Hormaza JI, Herrero M (2009) Global warming and sexual plant reproduction. Trends Plant Sci 14:30–36

    Article  PubMed  CAS  Google Scholar 

  • Herrero M, Dickinson HG (1981) Pollen-tube development in Petunia hybrida following compatible and incompatible intraspecific matings. J Cell Sci 47:365–383

    PubMed  CAS  Google Scholar 

  • Jain M, Prasad P, Boote K, Hartwell A, Chourey P (2007) Effects of season-long high temperature growth conditions on sugar-to-starch metabolism in developing microspores of grain sorghum (Sorghum bicolor L. Moench). Planta 227:67–79

    Article  PubMed  CAS  Google Scholar 

  • Johannsen MH, Stephenson AG (1998) Effects of temperature during microsporogenesis on pollen performance in Cucurbita pepo. Int J Plant Sci 159:616–626

    Article  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York

    Google Scholar 

  • Kong J, Li Z, Tan YP, Wan CX, Li SQ, Zhu YG (2007) Different gene expression patterns of sucrose–starch metabolism during pollen maturation in cytoplasmic male-sterile and male-fertile lines of rice. Physiol Plant 130:136–147

    Article  CAS  Google Scholar 

  • Lau TC, Stephenson AG (1993) Effects of soil nitrogen on pollen production, pollen grain size, and pollen performance in Cucurbita pepo (Cucurbitaceae). Am J Bot 80:763–768

    Article  CAS  Google Scholar 

  • Ledesma N, Sugiyama N (2005) Pollen quality and performance in strawberry plants exposed to high-temperature stress. J Am Soc Hortic Sci 130:341–347

    Google Scholar 

  • Lora J, Perez de Oteyza MA, Fuentetaja P, Hormaza JI (2006) Low temperature storage and in vitro germination of cherimoya (Annona cherimola Mill.) pollen. Sci Hortic 108:91–94

    Article  CAS  Google Scholar 

  • Lora J, Herrero M, Hormaza JI (2009a) The coexistence of bicellular and tricellular pollen in Annona cherimola (Annonaceae): implications for pollen evolution. Am J Bot 96:802–808

    Article  PubMed  Google Scholar 

  • Lora J, Testillano P, Risueno M, Hormaza J, Herrero M (2009b) Pollen development in Annona cherimola Mill. (Annonaceae). Implications for the evolution of aggregated pollen. BMC Plant Biol 9:129

    Article  PubMed  Google Scholar 

  • Lora J, Hormaza JI, Herrero M (2010) The progamic phase of an early-divergent angiosperm, Annona cherimola (Annonaceae). Ann Bot 105:221–231

    Article  PubMed  CAS  Google Scholar 

  • Lora J, Herrero M, Hormaza JI (2011) Stigmatic receptivity in a dichogamous early-divergent angiosperm species, Annona cherimola (Annonaceae): influence of temperature and humidity. Am J Bot 98:265–274

    Article  PubMed  Google Scholar 

  • Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434

    Article  PubMed  CAS  Google Scholar 

  • Marshall DL, Tyler AP, Abrahamson NJ, Avritt JJ, Barnes MG, Larkin LL, Medeiros JS, Reynolds J, Shaner MGM, Simpson HL, Maliakal-Witt S (2010) Pollen performance of Raphanus sativus (Brassicaceae) declines in response to elevated [CO(2)]. Sex Plant Reprod 23:325–336

    Article  PubMed  CAS  Google Scholar 

  • Nepi M, Franchi GG, Pacini E (2001) Pollen hydration status at dispersal: cytophysiological features and strategies. Protoplasma 216:171–180

    Article  PubMed  CAS  Google Scholar 

  • Nepi M, Cresti L, Guarnieri M, Pacini E (2010) Effect of relative humidity on water content, viability and carbohydrate profile of Petunia hybrida and Cucurbita pepo pollen. Plant Sys Evol 284:57–64

    Article  CAS  Google Scholar 

  • Pacini E (2010) Relationships between tapetum, loculus, and pollen during development. Int J Plant Sci 171:1–11

    Article  Google Scholar 

  • Pacini E, Guarnieri M, Nepi M (2006) Pollen carbohydrates and water content during development, presentation, and dispersal: a short review. Protoplasma 228:73–77

    Article  PubMed  CAS  Google Scholar 

  • Popenoe H (1989) Lost crops of the Incas: little known plants of the Andes with promise of worldwide cultivation. National Academy Press, Washington

    Google Scholar 

  • Poulton JL, Koide RT, Stephenson AG (2001a) Effects of mycorrhizal infection and soil phosphorus availability on in vitro and in vivo pollen performance in Lycopersicon esculentum (Solanaceae). Am J Bot 88:1786–1793

    Article  PubMed  CAS  Google Scholar 

  • Poulton JL, Koide RT, Stephenson AG (2001b) Effects of mycorrhizal infection, soil phosphorus availability and fruit production on the male function in two cultivars of Lycopersicon esculentum. Plant Cell Environ 24:841–849

    Article  Google Scholar 

  • Poulton JL, Bryla D, Koid RT, Stephenson AG (2002) Mycorrhizal infection and high soil phosphorus improve vegetative growth and the female and male functions in tomato. New Phytol 154:255–264

    Article  CAS  Google Scholar 

  • Prasad PVV, Craufurd PQ, Summerfield RJ (1999) Sensitivity of peanut to timing of heat stress during reproductive development. Crop Sci 39:1352–1357

    Article  Google Scholar 

  • Prasad PVV, Pisipati SR, Mutava RN, Tuinstra MR (2008) Sensitivity of grain sorghum to high temperature stress during reproductive development. Crop Sci 48:1911–1917

    Article  Google Scholar 

  • Prasad PVV, Boote KJ, Allen LH Jr (2011) Longevity and temperature response of pollen as affected by elevated growth temperature and carbon dioxide in peanut and grain sorghum. Environ Exp Bot 1:51–57

    Article  Google Scholar 

  • Pressman E, Peet MM, Pharr DM (2002) The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in the developing anthers. Ann Bot 90:631–636

    Article  PubMed  CAS  Google Scholar 

  • Rao GU, Jain A, Shivanna KR (1992) Effects of high temperature stress on Brassica pollen viability germination and ability to set fruits and seeds. Ann Bot 69:193–198

    Google Scholar 

  • Rosell P, Herrero M, Sauco VG (1999) Pollen germination of cherimoya (Annona cherimola Mill.). In vivo characterization and optimization of in vitro germination. Sci Hortic 81:251–265

    Article  CAS  Google Scholar 

  • Sabatini DD, Bensch K, Barrnett RJ (1963) Cytochemistry and electron microscopy—preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J Cell Biol 17:19–58

    Article  PubMed  CAS  Google Scholar 

  • Saini HS (1997) Effects of water stress on male gametophyte development in plants. Sex Plant Reprod 10:67–73

    Article  Google Scholar 

  • Schroeder CA (1971) Pollination of cherimoya. Calif Avocado Soc Yearb 44:119–122

    Google Scholar 

  • Scott RJ, Spielman M, Dickinson HG (2006) Stamen development: primordium to pollen. In: Jordan BR (ed) The molecular biology and biotechnology of flowering. CAB International, Wallingford, pp 298–331

    Chapter  Google Scholar 

  • Sears P (1926) The behaviour of pollen starch in a geranium and its bud sport. J Genet 17:33–42

    Article  Google Scholar 

  • Snider JL, Oosterhuis DM, Skulman BW, Kawakami EM (2009) Heat stress-induced limitations to reproductive success in Gossypium hirsutum. Physiol Plant 137:125–138

    Article  PubMed  CAS  Google Scholar 

  • Soria JT, Hermoso JM, Farre JM (1990) Polinización artificial del chirimoyo. Frutic Prof 35:15–22

    Google Scholar 

  • Speranza A, Calzoni GL, Pacini E (1997) Occurrence of mono- or disaccharides and polysaccharide reserves in mature pollen grains. Sex Plant Reprod 10:110–115

    Article  CAS  Google Scholar 

  • Stanley RG, Linkens HF (1974) Pollen: biology, biochemistry, management. Springer, Berlin

    Google Scholar 

  • Travers SE (1999) Pollen performance of plants in recently burned and unburned environments. Ecology 80:2427–2434

    Article  Google Scholar 

  • Wester PJ (1910) Pollination experiments with Anonas. Bull Torrey Bot Club 37:529–539

    Article  Google Scholar 

  • Young HJ, Stanton ML (1990) Influence of environmental quality on pollen competitive ability in wild radish. Science 248:1631–1632

    Article  PubMed  CAS  Google Scholar 

  • Zona S (2001) Starchy pollen in commelinoid monocots. Ann Bot 87:109–116

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank Afif Hedhly for help with the statistical analysis. Financial support for this work was provided by the Spanish Ministry of Science and Innovation—European Regional Development Fund (Project Grants AGL2009-12621-CO-01 and AGL2010-15140), INIA (RF2009-00010), GIE-Aragón 43, Junta de Andalucía (FEDER AGR2742), and the European Union under the INCO-DEV program (Contract 015100). J.L. was supported by a grant from Junta de Andalucía.

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Communicated by Hugh Dickinson.

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Lora, J., Herrero, M. & Hormaza, J.I. Pollen performance, cell number, and physiological state in the early-divergent angiosperm Annona cherimola Mill. (Annonaceae) are related to environmental conditions during the final stages of pollen development. Sex Plant Reprod 25, 157–167 (2012). https://doi.org/10.1007/s00497-012-0187-2

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