Skip to main content
Log in

A Comparative Study between Evergreen and Deciduous Daylily Species Reveals the Potential Contributions of Winter Shoot Growth and Leaf Freezing Tolerance to Foliar Habits

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Evergreen ornamental plants can supply year-round aesthetic value and strong ecological benefits in comparison to deciduous species. However, less attention has been paid to the cause of foliar habits, especially in herbaceous perennials. A comparative study on evergreen and deciduous species with close relationships could help to uncover the factors that determine foliar habits when sibling mutants are absent. Three independent experiments were conducted in the present study. Experiment 1 was focused on the changes in the percentage of green leaves (PGL) between evergreen daylilies (Hemerocallis aurantiaca Baker) and the deciduous species (Hemerocallis fulva L.). The results showed that their foliar habits were consistent with those of previous reports but could be influenced dramatically by the air temperature. The leaf freezing tolerance (LFT) and relevant morphological, physiological and biochemical variations in leaf tissues in addition to the shoot growth status were determined during Experiments 2 and 3 when comparing natural cold acclimation to de-acclimation. Correlation analyses between the PGL and other indices indicated that the winter shoot growth probably maintained the green leaves of the evergreen daylilies, while a strong LFT might facilitate the defoliation of deciduous species. Furthermore, the dormant deciduous daylily is more freezing-tolerant than the ever-growing evergreen species. This study also possesses practical value for plants with variant green periods in landscaping.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

DIA:

Digital image analysis

EL:

Electrolyte leakage

GDD:

Growing degree days

HSB:

Hue, saturation and brightness

LFT:

Leaf freezing tolerance

LT:

Low temperature

LT50 :

Lethal temperature causing 50% injury

LW:

Leaf width

MDA:

Malondialdehyde

NFL:

Number of the functional leaves

PGL:

Percentage of green leaves

RCC:

Relative chlorophyll content

REC:

Relative electrolyte conductivity

ROS:

Reactive oxygen species

SD:

Short-day

SER:

Shoot elongation rate

SOD:

Superoxide dismutase

SP:

Soluble protein

TSS:

Total soluble sugar

WC:

Water content

References

  • Adams WW, Zarter CR, Ebbert V, Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. AIBS Bull 54:41–49

    Google Scholar 

  • Anderson JV (2015) Advances in Plant Dormancy. Springer, Cham, pp 51–186

    Google Scholar 

  • Arora R, Wisniewski ME (1994) Cold acclimation in genetically related (sibling) deciduous and evergreen peach A 60-kilodalton bark protein in cold acclimated tissues of peach is heat stable and related to the dehydrin family of proteins. Plant Physiol 105:95–101

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arora R, Wisniewski ME, Scorza R (1992) Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica Batsch). Plant Physiol 99:1562–1568

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arora R, Wisniewski M, Rowland LJ (1996) Cold acclimation and alterations in dehydrin-like and bark storage proteins in the leaves of sibling deciduous and evergreen peach. J Am Soc Hortic Sci 121:915–919

    CAS  Google Scholar 

  • Bauerle WL, Oren R, Way DA, Qian SS, Stoy PC, Thornton PE, Bowden JD, Hoffman FM, Reynolds RF (2012) Photoperiodic regulation of the seasonal pattern of photosynthetic capacity and the implications for carbon cycling. Proc Nat Acad Sci USA 109:8612–8617

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baxter G (1999) Hemerocallis Check List 1994–1998. Am Hemericallis Soc

  • Bertrand A, Bipfubusa M, Claessens A, Rocher S, Castonguay Y (2017) Effect of photoperiod prior to cold acclimation on freezing tolerance and carbohydrate metabolism in alfalfa (Medicago sativa L). Plant Sci 264:122–128

    CAS  PubMed  Google Scholar 

  • Brummer EC, Shah MM, Luth D (2000) Reexamining the relationship between fall dormancy and winter hardiness in alfalfa. Crop Sci 40:971–977

    Google Scholar 

  • Charrier G, Améglio T (2011) The timing of leaf fall affects cold acclimation by interactions with air temperature through water and carbohydrate contents. Environ Exp Bot 72:351–357

    Google Scholar 

  • Chen Y, Jiang J, Chang Q, Gu C, Song A, Chen S, Dong B, Chen F (2014) Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species. Mol Biol Rep 41:815–822

    CAS  PubMed  Google Scholar 

  • Chen J, Han G, Shang C, Li J, Zhang H, Liu F, Wang J, Liu H, Zhang Y (2015) Proteomic analyses reveal differences in cold acclimation mechanisms in freezing-tolerant and freezing-sensitive cultivars of alfalfa. Front Plant Sci 6:105

    PubMed  PubMed Central  Google Scholar 

  • Chen J, Yang X, Huang X, Duan S, Long C, Chen J, Rong J (2017) Leaf transcriptome analysis of a subtropical evergreen broadleaf plant, wild oil-tea camellia (Camellia oleifera), revealing candidate genes for cold acclimation. BMC Genom 18:211

    Google Scholar 

  • Chianucci F, Lucibelli A, Dell’Abate MT (2018) Estimation of ground canopy cover in agricultural crops using downward-looking photography. Biosys Eng 169:209–216

    Google Scholar 

  • China Flora (1985) The flora of China, 16th edn. Sci Press, Beijing

    Google Scholar 

  • Daylily online database. (2015). Am Hemericallis Soc. https://daylilies.org/DaylilyDB/. Accessed 12 Dec 2015

  • Die JV, Arora R, Rowland LJ (2017) Proteome dynamics of cold-acclimating Rhododendron species contrasting in their freezing tolerance and thermonasty behavior. PLoS ONE 12:e0177389

    PubMed  PubMed Central  Google Scholar 

  • Ebdon JS, Gagne RA, Manley RC (2002) Comparative cold tolerance in diverse turf quality genotypes of perennial ryegrass. HortScience 37(5):826–830

    Google Scholar 

  • Edwards EJ, de Vos JM, Donoghue MJ (2015) Doubtful pathways to cold tolerance in plants. Nature 521:E5

    CAS  PubMed  Google Scholar 

  • Ellsworth PZ, Sternberg LSL (2015) Seasonal water use by deciduous and evergreen woody species in a scrub community is based on water availability and root distribution. Ecohydrology 8:538–551

    Google Scholar 

  • Erdal S, Genisel M, Turk H, Dumlupinar R, Demir Y (2015) Modulation of alternative oxidase to enhance tolerance against cold stress of chickpea by chemical treatments. J Plant Physiol 175:95–101

    CAS  PubMed  Google Scholar 

  • Ershadi A, Karimi R, Mahdei KN (2016) Freezing tolerance and its relationship with soluble carbohydrates, proline and water content in 12 grapevine cultivars. Acta Physiol Plant 38:2

    Google Scholar 

  • Estiarte M, Peñuelas J (2015) Alteration of the phenology of leaf senescence and fall in winter deciduous species by climate change: effects on nutrient proficiency. Global Change Biol 21:1005–1017

    Google Scholar 

  • Fuller MP, Wisniewski M (1998) The use of infrared thermal imaging in the study of ice nucleation and freezing of plants. J Therm Biol 23:81–89

    Google Scholar 

  • Garbero M, Andrade A, Reinoso H, Fernández B, Cuesta C, Granda V, Escudero C, Abdala G, Pedranzani H (2012) Differential effect of short-term cold stress on growth, anatomy, and hormone levels in cold-sensitive versus -resistant cultivars of Digitaria eriantha. Acta Physiol Plant 34:2079–2091

    CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314

    CAS  PubMed  Google Scholar 

  • Givnish TJ (2002) Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fenn 36:703–743

    Google Scholar 

  • González-Zurdo P, Escudero A, Babiano J, García-Ciudad A, Mediavilla S (2016) Costs of leaf reinforcement in response to winter cold in evergreen species. Tree Physiol 36:273–286

    PubMed  PubMed Central  Google Scholar 

  • Guo HL, Liu J, Zhu XH, Guo AG (2006) Evaluation of cold resistance of zoysia hybrids. Acta Agrestia Sinica 14:24–28

    Google Scholar 

  • Guo H, Xuan J, Liu J, Zhang Y, Zheng Y (2012) Association of molecular markers with cold tolerance and green period in zoysiagrass (Zoysia Willd.). Breed Sci 62:320–327

    PubMed  PubMed Central  Google Scholar 

  • Haagenson DM, Cunningham SM, Volenec JJ (2003) Root physiology of less fall dormant, winter hardy alfalfa selections. Crop Sci 43:1441–1447

    Google Scholar 

  • Hu JB, Dai MX, Peng ST (2018) An automated (novel) algorithm for estimating green vegetation cover fraction from digital image: UIP-MGMEP. Environ Monit Assess 190:687

    CAS  PubMed  Google Scholar 

  • Hughes NM, Neufeld HS, Burkey KO (2005) Functional role of anthocyanins in high-light winter leaves of the evergreen herb Galax urceolata. New Phytol 168:575–587

    CAS  PubMed  Google Scholar 

  • Janda T, Majláth I, Szalai G (2014) Interaction of temperature and light in the development of freezing tolerance in plants. J Plant Growth Regul 33:460–469

    CAS  Google Scholar 

  • Kamenetsky R, Okubo H (2012) Ornamental geophytes: from basic science to sustainable production. CRC Press, Florida

    Google Scholar 

  • Kikuzawa K, Lechowicz MJ (2011) Foliar habit and leaf longevity. Springer, Tokyo, pp 1–6

    Google Scholar 

  • Li HS (2000) Principles and technology of plant physiology and biochemistry experiments, 1st edn. Higher Education Press, Beijing

    Google Scholar 

  • Li Z, Reighard GL, Abbott AG, Bielenberg DG (2009) Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. J Exp Bot 60:3521–3530

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Alarcón-Zúñiga B, Kang J, Tahir N, Hammad M, Jiang Q, Wei Y, Reyno R, Robins JG, Brummer EC (2015) Mapping fall dormancy and winter injury in tetraploid alfalfa. Crop Sci 55:1995–2011

    CAS  Google Scholar 

  • Li D, Zhang J, Zhang J, Li K, Xia Y (2017) Green period characteristics and foliar cold tolerance in 12 iris species and cultivars in the Yangtze Delta, China. HortTechnology 27:399–407

    Google Scholar 

  • Lou X, Lv W, Wu Y, Zhou Y, Zhang W (2015) Preliminary study on cold hardiness of Hippeastrum and Amaryllis. North Hortic 3:81–83

    Google Scholar 

  • Lusk CH, Clearwater MJ, Laughlin DC, Harrison SP, Prentice LC, Nordenstahl M, Smith B (2018) Frost and leaf-size gradients in forests: global patterns and experimental evidence. New Phytol 219:565–573

    PubMed  Google Scholar 

  • Maillard A, Diquélou S, Billard V, Laîné P, Garnica M, Prudent M, Garcia-Mina J-M, Yvin J-C, Ourry A (2015) Leaf mineral nutrient remobilization during leaf senescence and modulation by nutrient deficiency. Front Plant Sci 6:317

    PubMed  PubMed Central  Google Scholar 

  • Motulsky H, Christopoulos A (2004) Fitting models to biological data using linear and nonlinear regression: a practical guide to curve fitting. Oxford University Press, New York

    Google Scholar 

  • Munné-Bosch S, Alegre L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Funct Plant Biol 31:203–216

    PubMed  Google Scholar 

  • Munshaw GC, Ervin EH, Beasley JS, Shang C, Zhang X, Parrish DJ (2010) Effects of late-season ethephon applications on cold tolerance parameters of four bermudagrass cultivars. Crop Sci 50:1022–1029

    CAS  Google Scholar 

  • Okeyo DO, Fry JD, Bremer D, Rajashekar CB, Kennelly M, Chandra A, Genovesi DA, Engelke MC (2011) Freezing tolerance and seasonal color of experimental zoysiagrasses. Crop Sci 51:2858–2863

    Google Scholar 

  • Patrignani A, Ochsner TE (2015) Canopeo: a powerful new tool for measuring fractional green canopy cover. Agron J 107:2312–2320

    CAS  Google Scholar 

  • Patton AJ, Hardebeck GA, Williams DW, Reicher ZJ (2004) Establishment of bermudagrass and zoysiagrass by seed. Crop Sci 44:2160–2167

    Google Scholar 

  • Pompeiano A, Grossi N, Guglielminetti L, Volterrani M (2014) Winter color retention and spring green-up of zoysiagrass genotypes in southern Europe. Europ J Hortic Sci 79:158–166

    Google Scholar 

  • Rodriguez J, Sherman WB, Scorza R, Wisniewski M, Okie WR (1994) ‘Evergreen’peach, its inheritance and dormant behavior. J Am Soc Hortic Sci 119:789–792

    Google Scholar 

  • Rubio S, Dantas D, Bressan-Smith R, Pérez FJ (2016) Relationship between endodormancy and cold hardiness in grapevine buds. J Plant Growth Regul 35:266–275

    CAS  Google Scholar 

  • Serena M, Schiavon M, Sallenave R, Leinauer B (2018) Nitrogen fertilization of warm-season turfgrasses irrigated with saline water from varying irrigation systems. 1. Quality, spring green-up and fall colour retention. J Agron Crop Sci 204:252–264

    CAS  Google Scholar 

  • Sønsteby A, Heide OM (2008) Environmental control of growth and flowering of Rubus idaeus L. cv. Glen Ample. Sci Horticult 117:249–256

    Google Scholar 

  • Sønsteby A, Heide OM (2014) Cold tolerance and chilling requirements for breaking of bud dormancy in plants and severed shoots of raspberry (Rubus idaeus L). J Horticult Sci Biotechnol 89:631–638

    Google Scholar 

  • Streich A, Steinegger D (2000) G00–1412 Daylilies.

  • Tarkowski ŁP, Van den Ende W (2015) Cold tolerance triggered by soluble sugars: a multifaceted countermeasure. Front Plant Sci 6:203

    PubMed  PubMed Central  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol 50:571–599

    CAS  Google Scholar 

  • Thomashow MF (2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol 154:571–577

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson MM, Smith DC, Burgess JE (1985) Nondormant mutants in a temperate tree species, Corylus avellana L. Theor Appl Genet 70:687–692

    CAS  PubMed  Google Scholar 

  • Trischuk RG, Schilling BS, Low NH, Gray GR, Gusta LV (2014) Cold acclimation, de-acclimation and re-acclimation of spring canola, winter canola and winter wheat: the role of carbohydrates, cold-induced stress proteins and vernalization. Environ Exp Bot 106:156–163

    CAS  Google Scholar 

  • Vitasse Y, Lenz A, Körner C (2014) The interaction between freezing tolerance and phenology in temperate deciduous trees. Front Plant Sci 5:541

    PubMed  PubMed Central  Google Scholar 

  • Wang D, Xuan J, Guo H, Liu J (2011) Seasonal changes of freezing tolerance and its relationship to the contents of carbohydrates, proline, and soluble protein of Zoysia. Acta Pratac Sin 4:013

    Google Scholar 

  • Wang Q, Cheng T, Yu X, da Silva JAT, Byrne DH (2014) Physiological and biochemical responses of six herbaceous peony cultivars to cold stress. S Afr J Bot 94:140–148

    CAS  Google Scholar 

  • Welling A, Moritz T, Palva ET, Junttila O (2002) Independent activation of cold acclimation by low temperature and short photoperiod in hybrid aspen. Plant Physiol 129:1633–1641

    CAS  PubMed  PubMed Central  Google Scholar 

  • White RH, Schmidt RE (1990) Fall performance and post-dormancy growth of ‘Midiron’ bermudagrass in response to nitrogen, iron, and benzyladenine. J Am Soc Hortic Sci 115:57–61

    CAS  Google Scholar 

  • Wisniewski M, Gusta LV, Fuller MP, Karlson D (2009) Ice nucleation, propagation and deep supercooling: the lost tribes of freezing studies. In: Gusta LV, Wisniewski ME, Tanino KK (eds) Plant cold hardiness: from the laboratory to the field. CABI, Cambridge, pp 73–97

    Google Scholar 

  • Wisniewski M, Norelli J, Artlip T (2015) Overexpression of a peach CBF gene in apple: a model for understanding the integration of growth, dormancy, and cold hardiness in woody plants. Front Plant Sci 6:85

    PubMed  PubMed Central  Google Scholar 

  • Wooten J (1972) Performance of modern, named daylilies in South Florida. Proc Fla Hortic Soc 85:438–440

    Google Scholar 

  • Wu Y, Sun M, Zhang J, Zhang L, Ren Z, Min R, Wang X, Xia Y (2019) Differential effects of Paclobutrazol on the bulblet growth of oriental lily cultured in vitro: growth behavior, carbohydrate metabolism, and antioxidant capacity. J Plant Growth Regul 38:359–372

    CAS  Google Scholar 

  • Xu XG, Wu YQ (2000) Discussion on reason and countermeasure of turning yellow of warm-season turfgrass in winter. Pratac Sci 17:43–49

    Google Scholar 

  • Yang C, Li D, Mao D, Liu X, Ji C, Li X, Zhao X, Cheng Z, Chen C, Zhu L (2013) Overexpression of micro RNA 319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L). Plant Cell Environ 36:2207–2218

    CAS  PubMed  Google Scholar 

  • Yang Y, Jia Z, Chen F, Sang Z, Ma L (2015) Comparative analysis of natural cold acclimation and deacclimation of two Magnolia species with different winter hardiness. Acta Physiol Plant 37:129

    CAS  Google Scholar 

  • Yue C, Cao HL, Wang L, Zhou YH, Huang YT, Hao XY, Wang YC, Wang B, Yang YJ, Wang XC (2015) Effects of cold acclimation on sugar metabolism and sugar-related gene expression in tea plant during the winter season. Plant Mol Biol 88:591–608

    CAS  PubMed  Google Scholar 

  • Zhang Q, Zhu C, Jiang T, Becker S (2005) Mid-Pleistocene environmental reconstruction based on Xiashu loess deposits in the Yangtze Delta, China. Quat Int 135:131–137

    Google Scholar 

  • Zhang LL, Zhao MG, Tian QY, Zhang WH (2011) Comparative studies on tolerance of Medicago truncatula and Medicago falcata to freezing. Planta 234:445–457

    CAS  PubMed  Google Scholar 

  • Zhang J, Wu D, Xia Y (2013a) Landscape application and wild resource investigation of evergreen perennials in Zhejiang province. Chin Landsc Archit 10:018

    Google Scholar 

  • Zhang L, Liu M, Qiao G, Jiang J, Jiang Y, Zhuo R (2013b) Transgenic poplar “NL895” expressing CpFATB gene shows enhanced tolerance to drought stress. Acta Physiol Plant 35:603–613

    CAS  Google Scholar 

  • Zhang X, Shang C, Liu Y, Hu G, Harich K, Ervin EH (2017) Hormone and dehydrin expression responses to cold acclimation in two zoysiagrass cultivars with contrasting freezing tolerance. Int Turf Soc Res J 13:547–555

    Google Scholar 

  • Zhang Q, Zhang H, Sun L, Fan G, Ye M, Jiang L, Liu X, Ma K, Shi C, Bao F (2018) The genetic architecture of floral traits in the woody plant Prunus mume. Nature Commun 9:1702

    Google Scholar 

Download references

Acknowledgements

This work was supported by Major Agricultural Technology Cooperative Promotion Plan of Zhejiang Province (2018XTTGHH01).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jiaping Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, D., Xia, Y., Lou, J. et al. A Comparative Study between Evergreen and Deciduous Daylily Species Reveals the Potential Contributions of Winter Shoot Growth and Leaf Freezing Tolerance to Foliar Habits. J Plant Growth Regul 39, 1030–1045 (2020). https://doi.org/10.1007/s00344-019-10042-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-019-10042-x

Keywords

Navigation