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Warm temperature conditions restrict the sexual reproduction and vegetative growth of the spring ephemeral Gagea lutea (Liliaceae)

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Abstract

The responses of reproduction and growth to climate warming are important issues to predict the fate of plant populations at high latitudes. Spring ephemerals inhabiting cool-temperate forests grow better under cool conditions, but how reproductive performance is influenced by warm weather is unclear. The phenological and physiological responses of reproduction and vegetative growth to warm temperature and light conditions were evaluated in the spring ephemeral Gagea lutea. Leaf and bract physiological activities, bulb growth, and seed production were compared among reproductive plants grown in forest, open, and greenhouse (GH; warming manipulation in the open site) plots. In vitro pollen germination ability was tested under various temperatures. In the GH, leaf and bract photosynthetic activities decreased rapidly at the fruiting stage, but dark respiration rates remained high, resulting in higher carbon exhaust in warm conditions. Both leaf and bract sizes and their longevities were reduced in the GH. Annual bulb growth was largest in the forest plot and smallest in the GH plot. Pollen germination was strongly inhibited at high temperature (30 °C). Fruit and seed productions were decreased only in the GH plot. Both vegetative and reproductive activities were negatively affected by warm temperature, resulting in less vegetative growth and lower seed-set, whereas an understory habitat was beneficial for vegetative growth and showed similar seed production to an open habitat over the experimental period. Decreasing population dynamics of spring ephemerals was predicted in response to future warming climate not only by growth inhibition but also by restriction of seed production.

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References

  • Badri MA, Minchin PEH, Lapointe L (2007) Effects of temperature on the growth of spring ephemerals: Crocus vernus. Physiol Plant 130:67–76

    Article  CAS  Google Scholar 

  • Bernatchez A, Lapointe L (2012) Cooler temperatures favour growth of wild leek (Allium tricoccum), a deciduous forest spring ephemeral. Botany 90:1125–1132

    Article  CAS  Google Scholar 

  • Constable JVH, Peffer BJ, DeNicola DM (2007) Temporal and light-based changes in carbon uptake and storage in the spring ephemeral Podophyllum peltatum (Berberidaceae). Env Exp Bot 60:112–120

    Article  CAS  Google Scholar 

  • Devasirvatham V, Tan DKY, Gaur PM, Raju TN, Trethowan RM (2012) High temperature tolerance in chickpea and its implications for plant improvement. Crop Pasture Sci 63:419–428

    Article  Google Scholar 

  • Easterling DR et al (1997) Maximum and minimum temperature trends for the globe. Science 277:364–367

    Article  CAS  Google Scholar 

  • Fitter AH, Hay RKM (1987) Environmental physiology of plants, 2nd edn. Academic Press, London

    Google Scholar 

  • Fitter AH, Fitter RSR, Harris ITB, Williamson MH (1995) Relationships between first flowering date and temperature in the flora of a locality in central England. Funct Ecol 9:55–60

    Article  Google Scholar 

  • Gandin A, Gutjahr S, Dizengremel P, Lapointe L (2011) Source-sink imbalance increases with growth temperature in the spring geophyte Erythronium americanum. J Exp Bot 62:3467–3479

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gutjahr S, Lapointe L (2008) Carbon dioxide enrichment does not reduce leaf longevity or alter accumulation of carbon reserves in the woodland spring ephemeral Erythronium americanum. An Bot 102:835–843

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hedhly A, Hormaza JI, Herrero M (2008) Global warming and sexual plant reproduction. Trend Plant Sci 14:30–36

    Article  Google Scholar 

  • Ida TY, Kudo G (2008) Timing of canopy closure influences carbon translocation and seed production of an understory herb, Trillium apetalon (Trilliaceae). Ann Bot 101:435–446

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ida TY, Harder LD, Kudo G (2013) Demand-driven resource investment in annual seed production by a perennial angiosperm precludes resource limitation. Ecology 94:51–61

    Article  PubMed  Google Scholar 

  • Iglesias DJ, Lliso I, Tadeo FR, Talon M (2002) Regulation of photosynthesis through source: sink imbalance in citrus is mediated by carbohydrate content in leaves. Physiol Plant 116:563–572

    Article  CAS  Google Scholar 

  • Ishii HS, Sakai S (2000) Optimal timing of corolla abscission: experimental study on Erythronium japonicum (Liliaceae). Funct Ecol 14:122–128

    Article  Google Scholar 

  • Kakani VG, Reddy KR, Koti S, Wallace TP, Prasad PVV, Reddy VR, Zhao D (2005) Differences in in vitro pollen germination and pollen tube growth of cotton cultivars in response to high temperature. Ann Bot 96:59–67

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kaushal NA, Rashmi AA, Gupta KA, Pooran GB, Kadambot HM, Siddique C, Harsh NAD (2013) Heat-stress-induced reproductive failures in chickpea (Cicer arietinum) are associated with impaired sucrose metabolism in leaves and anthers. Funct Plant Biol 40:1334–1349

    Article  CAS  Google Scholar 

  • Kudo G, Nishikawa Y, Kasagii T, Kosuge S (2004) Does seed production of spring ephemerals decrease when spring comes early? Ecol Res 19:255–259

    Article  Google Scholar 

  • Kudo G, Ida TY, Tani T (2008) Linkages between phenology, pollination, photosynthesis, and reproduction in deciduous forest understory plants. Ecology 89:321–331

    Article  PubMed  Google Scholar 

  • Lapointe L (2001) How phenology influences physiology in deciduous forest spring ephemerals. Physiol Plant 113:151–157

    Article  CAS  PubMed  Google Scholar 

  • Lapointe L, Lerat S (2006) Annual growth of the spring ephemeral Erythronium americanum as a function of temperature and mycorrhizal status. Can J Bot 84:39–48

    Article  CAS  Google Scholar 

  • Lundmark M, Hurry V, Lapointe L (2009) Low temperature maximizes growth of Crocus vernus (L.) Hill via changes in carbon partitioning and corm development. J Exp Bot 60:2203–2213

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Menzel A (2000) Trends in phenological phases in Europe between 1951 and 1996. Int J Biomet 44:76–81

    Article  CAS  Google Scholar 

  • Menzel A (2002) Phenology: its importance to the global change community. Clim Change 54:379–385

    Article  Google Scholar 

  • Muller RN (1978) The phenology, growth, and ecosystem dynamics of Erythronium americanum in the northern hardwood forest. Ecol Monogr 48:1–20

    Article  Google Scholar 

  • Niesenbaum RA (1993) Light or pollen: seasonal limitations on female reproductive success in the understory shrub Lindera benzoin. J Ecol 81:315–323

    Article  Google Scholar 

  • Nishikawa Y (1998) The function of multiple flowers of a spring ephemeral, Gagea lutea (Liliaceae), with reference to blooming order. Can J Bot 76:1404–1411

    Google Scholar 

  • Nishikawa Y (2009) Significance of intra-inflorescence variation on flowering time of a spring ephemeral, Gagea lutea (Liliaceae), under seasonal fluctuations of pollinator and light availabilities. Plant Ecol 202:337–347

    Article  Google Scholar 

  • Price MV, Waser NM (1998) Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology 79:1261–1271

    Article  Google Scholar 

  • Primack RB (1985) Longevity of individual flowers. Ann Rev Ecol Syst 16:15–37

    Article  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Rothstein DE, Zak DR (2001) Photosynthetic adaptation and acclimation to exploit seasonal periods of direct irradiance in three temperate, deciduous-forest herbs. Funct Ecol 15:722–731

    Article  Google Scholar 

  • Routhier M, Lapointe L (2002) Impact of tree leaf phenology on growth rates and reproduction in the spring flowering species Trillium erectum (Liliaceae). Am J Bot 89:500–505

    Article  PubMed  Google Scholar 

  • Sawada S, Sato M, Kasai A, Yaochi D, Kameya Y, Matsumoto I, Kasai M (2003) Analysis of the feed-forward effects of sink activity on the photosynthetic source-sink balance in single-rooted sweet potato leaves. I. Activation of RuBPcase through the development of sinks. Plant Cell Physiol 44:190–197

    Article  CAS  PubMed  Google Scholar 

  • Schemske DW, Willson MF, Melampy MN, Miller LJ, Verner L, Schemske KM, Best LB (1978) Flowering ecology of some spring woodland herbs. Ecology 59:351–366

    Article  Google Scholar 

  • Schnittler M, Pfeiffer T, Harter D, Hamann A (2009) Bulbils contra seeds: reproductive investment in two species of Gagea (Liliaceae). Plant Syst Evol 279:29–40

    Article  Google Scholar 

  • Sparks TH, Jeffree EP, Jeffree CE (2000) An examination of the relationship between flowering times and temperature at the national scale using long-term phenological records from the UK. Int J Biometeor 44:82–87

    Article  CAS  Google Scholar 

  • Sunmonu N, Kudo G (2014) How do sink and source activities influence reproduction and vegetative growth of spring ephemeral herbs under different light conditions. J Plant Res 127:503–511

    Article  PubMed  Google Scholar 

  • Sunmonu N, Ida TY, Kudo G (2013) Photosynthetic compensation by the reproductive structures in the spring ephemeral Gagea lutea. Plant Ecol 214:175–188

    Article  Google Scholar 

  • Tardieu F, Reymond M, Hamard P, Granier C, Muller B (2000) Spatial distributions of expansion rate, cell division rate and cell size in maize leaves: a synthesis of the effects of soil water status, evaporative demand and temperature. J Exp Bot 51:1505–1514

    Article  CAS  PubMed  Google Scholar 

  • Vitasse Y, Porté AJ, Kremer A, Michalet R, Delzon S (2009) Responses of canopy duration to temperature changes in four temperate tree species: relative contribution of spring and autumn leaf phenology. Oecologia 161:187–198

    Article  PubMed  Google Scholar 

  • Whigham DF (2004) Ecology of woodland herbs in temperate deciduous forests. Ann Rev Ecol Evol Syst 35:583–621

    Article  Google Scholar 

  • Yoshie F (2008) Effects of growth temperature and winter duration on leaf phenology of a spring ephemeral (Gagea lutea) and a summergreen forb (Maianthemum dilatatum). J Plant Res 121:483–492

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Y. Amagai, J. Sinclair, D. Tika, J. Doddy, and K. TaeOh for their help in the snow removal exercise. This study was partly supported by a grant-in-aid from the Japan Society for the Promotion of Science [23405006].

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Authors and Affiliations

  1. Faculty of Environmental Earth Science, Hokkaido University, Sapporo, 060-0810, Japan

    Ninuola Sunmonu & Gaku Kudo

Authors
  1. Ninuola Sunmonu
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  2. Gaku Kudo
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Corresponding author

Correspondence to Gaku Kudo.

Additional information

Communicated by Erik P Hamerlynck.

Appendix

Appendix

See Fig. 6.

Fig. 6
figure 6

Soil temperature during the growth period in 2013 in each plot. Measurements were performed at the depth of 10 cm at hourly intervals

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See Tables 5 and 6.

Table 5 Results of generalized linear models for reproductive performance in open, forest, and greenhouse [GH] plots
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Table 6 Results of generalized linear models for pollen germination rate and pollen tube length in each temperature condition (10, 15, 20, 25, and 30 °C)
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Sunmonu, N., Kudo, G. Warm temperature conditions restrict the sexual reproduction and vegetative growth of the spring ephemeral Gagea lutea (Liliaceae). Plant Ecol 216, 1419–1431 (2015). https://doi.org/10.1007/s11258-015-0520-6

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  • DOI: https://doi.org/10.1007/s11258-015-0520-6

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