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Dormancy in Tilia miqueliana is attributable to permeability barriers and mechanical constraints in the endosperm and seed coat

  • Structural Botany - Original Article
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Abstract

Tilia miqueliana is in the genus Tilia (Tiliaceae [part of the Malvaceae per APGIII]) of the Malvales family. The mechanisms responsible for dormancy in T. miqueliana were investigated by exploring changes in seed coat permeability, seed water and endosperm content, and endogenous hormones during dormancy release and germination. The structure and permeability of the seed coat and endosperm were assessed using magnetic resonance imaging, scanning electron microscopy, and paraffin section detection. The biological activities of key enzymes in the oxidation pathway were evaluated. Soluble sugar and starch content was determined using the anthrone colorimetric method. Protein contents were determined using Coomassie Brilliant Blue G-250 staining, and the Soxhlet extraction method was used to determine fat content. The endogenous hormones abscisic acid (ABA), gibberellic acid (GA), and zeatin riboside (ZR) contents were determined using enzyme-linked immunosorbent assays. The results indicate that poor permeability and mechanical constraints in the seed coat and endosperm are the key mechanisms regulating dormancy in T. miqueliana seeds. The dormancy types are physical and physiological dormancy. Concentrated sulfuric acid (H2SO4) + gibberellic acid 3 (GA3) + cold stratification treatments rapidly induced dormancy and accelerated germination. Activation of the tricarboxylic acid cycle and pentose phosphate pathway were critical for respiration. The metabolism of starch, protein, and fat in the endosperm was accelerated. The expression of endogenous GA3, which promotes germination, increased, whereas that of ABA, which inhibits germination, decreased. The ratios of GA3/ABA and ZR/ABA increased. Our study provides a theoretical foundation for the development of breeding methods.

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Abbreviations

SEM:

Scanning electron microscopy

PSD:

Paraffin section detection

PGI:

Phosphohexose isomerase

MDH:

Malate dehydrogenase

TCA:

Tricarboxylic acid

G-6-PDH:

Glucose-6-phosphate dehydrogenase

6- PGDH:

6-Phosphogluconate dehydrogenase

ABA:

Abscisic acid

GA:

Gibberellic acid

ZR:

Zeatin riboside

H2SO4 :

Concentrated sulfuric acid

GA3 :

Gibberellic acid 3

HMRI:

High-field nuclear magnetic resonance imaging

SNR:

Signal–noise ratio

EMP:

Embden–Meyerhof–Parnas

PPP:

Pentose phosphate pathway

ATP:

Adenosine triphosphate

PY:

Physical dormancy

PD:

Physiological dormancy

References

  • Alencar WS, Acayanka E (2012) Lima EC (2020) Application of Mangifera indica (mango) seeds as a biosorbent for removal of Victazol Orange 3R dye from aqueous solution and study of the biosorption mechanism. Chem Eng J 209:577–588

    Article  CAS  Google Scholar 

  • Bergmeyer HU (1956) Methods of Enzymatic Analysis. Verlag Chemie G.m.b.H/Academic press, Weinheim/New York

    Google Scholar 

  • Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Bradford KJ, Kigel J, Galili G (1995) Water relations in seed germination. Seed Dev Ger 1:351–396

    Google Scholar 

  • Brown AP, Wray JL (1968) Correlated changes of some enzyme activities and cofactor and substrate contents of pea cotyledon tissue during germination. Biochem J 108:437–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cong S, Wang HB, Wang XD (2013) Respiratory changes during dormancy of grape buds. Sci Agric Sin 46:1201–1207

    CAS  Google Scholar 

  • Cruz LJ, Cagampang GB, Juliano BO (1970) Biochemical factors affecting protein accumulation in the rice grain. Plant Physiol 46:743–747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delefosse M, Povidisa K, Poncet D (2016) Variation in size and chemical composition of seeds from the seagrass Zostera marina ecological implications. Aquat Bot 131:7–14

    Article  Google Scholar 

  • Elmaki HB, Babiker EE, El Tinay AH (1999) Changes in chemical composition, grain malting, starch and tannin contents and protein digestibility during germination of sorghum cultivars. Food Chem 64:331–336

    Article  CAS  Google Scholar 

  • Erbaş S, Tonguç M, Şanli A (2016) Mobilization of seed reserves during germination and early seedling growth of two sunflower cultivars. J Appl Bot Food Qual 89:217–222

    Google Scholar 

  • Galland M, He D, Lounifi I (2017) An integrated “multi-omics” comparison of embryo and endosperm tissue-specific features and their impact on rice seed quality. Front Plant Sci 8:1–23

    Article  Google Scholar 

  • Ghose TK (1987) Measurement of cellulase activities. Pure Appl Chem 59:257–268

    Article  CAS  Google Scholar 

  • Hemalatha KPJ, Prasad DS (2003) Changes in the metabolism of protein during germination of sesame (Sesamum indicum L.) seeds. Plant Food Hum Nutr 58:1–10

    Article  Google Scholar 

  • Holmes WS, Ooi MPL, Kuang YC (2020) Signal-to-Noise Ratio contributors and effects in proximal Near-Infrared spectral reflectance measurement on plant leaves. In: 2020 IEEE International Instrumentation and Measurement Technology Conference (I2MTC), pp 1–6

  • Li L, Lv F, Guo Y (2016) Respiratory pathway metabolism and energy metabolism associated with senescence in postharvest Broccoli (Brassica oleracea L. var. italica) florets in response to O2/CO2 controlled atmospheres. Postharvest Biol Tec 111:330–336

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Sawhney VK, Steeves TA (1993) Staining of paraffin-embedded plant material in safranin and fast green without prior removal of the paraffin. Can J Bot 71(7):996–999

    Article  CAS  Google Scholar 

  • Née G, Xiang Y, Soppe WJJ (2017) The release of dormancy, a wake-up call for seeds to germinate. Curr Opin Plant Biol 35(2017):8–14

    Article  PubMed  Google Scholar 

  • Ning W, Fan WL (2006) Effect of alternating temperature and gibberellin (GA3) on metabolic control of Japanese Aralia (Araliaelata) seed in dormancy-breaking process. Acta Hort Sin 33:649–652

    CAS  Google Scholar 

  • Obroucheva NV, Sinkevich IA, Lityagina SV (2017) Water relations in germinating seeds. Russ J Plant Physl 64:625–633

    Article  CAS  Google Scholar 

  • Palmiano EP, Juliano BO (1972) Biochemical changes in the rice grain during germination. Plant Physiol 49:51–756

    Article  Google Scholar 

  • Rolston MP (1978) Water impermeable seed dormancy. Bot Rev 44:365–396

    Article  CAS  Google Scholar 

  • Rosental L, Nonogaki H (2014) Activation and regulation of primary metabolism during seed germination. Seed Sci Res 24:1–15

    Article  CAS  Google Scholar 

  • Ross GJD (1980) Pentose phosphate metabolism during dormancy breakage in Corylus avellana L. Planta 148:362–366

    Article  PubMed  Google Scholar 

  • Satyanrayana B, Devi PS, Arundathi A (2011) Biochemical changes during seed Germination of Sterculia urens Roxb. Not Sci Biol 3:105–108

    Article  Google Scholar 

  • Shi FH, Shen YB (2012) Protection, development and utilization of Tilia miqueliana seeds. J for Eng 26:11–14

    Google Scholar 

  • Shi FH, Zhu CC (2008) Germination and dormancy of Tilia miqueliana seeds. J for Env 28:48–51

    CAS  Google Scholar 

  • Shutov AD, Vaintraub IA (1987) Degradation of storage proteins in germinating seeds. Phytochemistry 26:1557–1566

    Article  CAS  Google Scholar 

  • Soriano D, Huante P, Gamboa-deBuen A (2014) Effects of burial and storage on germination and seed reserves of 18 tree species in a tropical deciduous forest in Mexico. Oecologia 174:33–34

    Article  PubMed  Google Scholar 

  • Sreenivasulu N, Usadel B, Winter A (2008) Barley grain maturation and germination: metabolic pathway and regulatory network commonalities and differences highlighted by new mapman/pageman profiling tools. Plant Physiol 146:1738–1758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swamy PM, Sandhyarani CK (1986) Contribution of the pentose phosphate pathway and glycolytic pathway to dormancy breakage and germination of peanut (Arachis hypogaea L.) seeds. J Exp Bot 37:80–88

    Article  CAS  Google Scholar 

  • Tang SJ (2008) Research on the ecology and garden application of Tilia miqueliana. Nanjing Fore Univ 2008:1–139

    Google Scholar 

  • Taylor KA (1995) A modification of the phenol/sulfuric acid assay for total carbohydrates giving more comparable absorbances. Appl Biochem Biotech 53:207–214

    Article  CAS  Google Scholar 

  • Taylor JRN, Robbins DJ (1993) Factors influencing beta-amylase activity in sorghum malt. J I Brewing 99:413–416

    Article  CAS  Google Scholar 

  • Tuo-ming XU, Bing-qiang T, Zhi-da SUN (2011) Changes of three main nutrient during oat germination. Nat Prod Res Dev 439:534–537

    Google Scholar 

  • Vergara R, Pérez FJ (2010) Similarities between natural and chemically induced bud-endodormancy release in grapevine Vitis vinifera L. Sci Hortic-Amsterdam 125:648–653

    Article  CAS  Google Scholar 

  • Wang Y, Li B, Du M (2012) Mechanism of phytohormone involvement in feedback regulation of cotton leaf senescence induced by potassium deficiency. J Exp Bot 63:5887–5901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XK (2006) Principles and techniques of plant physiological and biochemical experiment. Higher Education Press, Beijing, pp 174–176

    Google Scholar 

  • Wu Y, Shen YB (2021) The structural and chemical characteristics of the pericarp are important in Tilia miqueliana seed dormancy. New for 2021:1–14

    CAS  Google Scholar 

  • Yang YH (2009) Study on the Metabolism of endosperm substances in Tilia miqueliana seed dormancy release. Nanjing Univ 2009:1–60

    Google Scholar 

  • Yang P, Li X, Wang X (2007) Proteomic analysis of rice (Oryza sativa) seeds during germination. Proteomics 7:3358–3368

    Article  CAS  PubMed  Google Scholar 

  • Yanmei W, Lijun W, Bing Y (2018) Changes in ABA, IAA, GA3, and zr levels during seed dormancy release in idesia polycarpa maxim from Jiyuan. Pol J Environ Stud 27:1833–1839

    Article  CAS  Google Scholar 

  • Yu M, Xu H, Zhang H (2016) Regulation of plant hormones on seed dormancy and germination. Plant Physiol 52:599–606

    CAS  Google Scholar 

  • Yuxi Z, Dan Y, Chunying L (2018) Dynamic of carbohydrate metabolism and the related genes highlights PPP pathway activation during chilling induced bud dormancy release in tree peony (Paeonia suffruticosa). Sci Hortic-Amsterdam 242:36–43

    Article  CAS  Google Scholar 

  • Zhang SL (2008) Effects of salicylic acid on respiratory pathway of Huang-guan Pear (D), (Master Thesis). Hebei Agr Univ 2008(1):1–45

    Google Scholar 

  • Zhao YH, Liu HQ (2000) Affection of respiratory inhibitor NaN3 oil dormancy relieving and germination of Panax quinquefolium seed and its synegistic effect with low temperature. Prim J Chin Mate Med 14:6–7

    CAS  Google Scholar 

  • Zhao J, Li G, Yi GX, Wang BM, Deng AX, Nan TG (2006) Comparison between conventional indirect competitive enzyme-linked immunosorbent assay (icELISA) and simplified icELISA for small molecules. Anal Chim Acta 571:79–85

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank the College of Forestry, Nanjing Forestry University, and Co-innovation Center for Sustainable Forestry in Southern China, Southern Tree Inspection Center National Forestry Administration.

Funding

This work was supported by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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Authors and Affiliations

  1. College of Forestry, Nanjing Forestry University, Nanjing, Jiangsu, China

    Yu Wu & YongBao Shen

  2. Co-innovation Center for Sustainable Forestry in Southern China, Southern Tree Inspection Center National Forestry Administration, Nanjing, Jiangsu province, China

    YongBao Shen

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  1. Yu Wu
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Contributions

YBS conceived the original screening and research plans; YW performed the experiments; YW designed the experiments and analyzed the data; YW conceived the project and wrote the article with contributions of all the authors. YW agrees to serve as the author responsible for contact and ensures communication. All authors have read and approved the manuscript.

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Correspondence to YongBao Shen.

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Wu, Y., Shen, Y. Dormancy in Tilia miqueliana is attributable to permeability barriers and mechanical constraints in the endosperm and seed coat. Braz. J. Bot 44, 725–740 (2021). https://doi.org/10.1007/s40415-021-00749-1

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  • DOI: https://doi.org/10.1007/s40415-021-00749-1

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