Skip to main content
SpringerLink
Log in

Elemental and biochemical markers of stigma receptivity in sunflower

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Stigma development in sunflower is accompanied with an accumulation of calcium (33 %), potassium (37 %) and boron (62 %) in mature stigma as compared to stigma at bud stage, thereby demonstrating their essential roles in attaining receptivity. Membrane-bound calcium accumulation is enhanced on the pellicle and is also evident in the cytoplasm accompanying stigma maturation. Total soluble carbohydrate content increases in the staminate stage (55 %) as compared to bud stage. Glucose and fructose are the major monosaccharides and their contents are maximum in the staminate stage. Total lipid content also increases with the passage of stigma development. Erucic acid (22:1) is expressed specifically in the bud and staminate stages. A variation in the contents of triacylglycerides and free fatty acids, and expression of fatty acyl esterases in mature stigma have been correlated with biochemical events associated with signalling mechanisms. Lastly, enhanced expression of two hydrolytic enzymes, namely β-1,3 glucanase and fatty acyl ester hydrolase, has been observed to correlate with stigma maturation. Present findings, thus, provide new information on the structural and biochemical changes marking various signalling events associated with successful pollen–stigma interaction.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Acar I, Ak BE, Sarpkaya K (2010) Effects of boron and gibberellic acid on in vitro pollen germination of pistachio (Pistacia vera L.). Afr J Biotechnol 9:5126–5130

    CAS  Google Scholar 

  • Al-Amery MM, Hamza JH, Fuller MP (2011) Effect of boron foliar application on reproductive growth of sunflower (Helianthus annuus L.). Int J Agron 230712. doi:10.1155/2011/230712

  • Allen AM, Lexer C, Hiscock SJ (2010) Comparative analysis of pistil transcriptomes reveals conserved and novel genes expressed in dry, wet, and semidry stigmas. Plant Physiol 154:1347–1360

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Allen AM, Thorogood CJ, Hegarty MJ, Lexer C, Hiscock SJ (2011) Pollen-pistil interactions and self-incompatibility in Asteraceae: new insights from studies of Senecio squalidus (Oxford ragwort). Ann Bot 108:687–698

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ameele RJ (1982) The transmitting tract in Gladiolus. 1. The stigma and the pollen–stigma interaction. Am J Bot 69:389–401

    Article  Google Scholar 

  • Ashley MK, Grant M, Grabov A (2006) Plant responses to potassium deficiencies: a role for potassium transport proteins. J Exp Bot 57:425–436

    Article  CAS  PubMed  Google Scholar 

  • Bednarska E (1989) Localization of calcium on the stigma surface of Ruscus aculeatus L. Planta 179:11–16

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharya A, Mandal S (2004) Pollination, pollen germination and stigma receptivity in Moringa oleifera Lamk. Grana 43:48–56

    Google Scholar 

  • Bílková J, Albrechtová J, Opatrná J (1999) Histochemical detection and image analysis of non-specific esterase activity and the amount of polyphenols during annual bud development in Norway spruce. J Exp Bot 50:1129–1138

    Article  Google Scholar 

  • Bolaños L, Lukaszewski K, Bonilla I, Blevins D (2004) Why boron? Plant Physiol Biochem 42:907–912

    Article  PubMed  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 

  • Bucciaglia PA, Zimmermann E, Smith AG (2003) Functional analysis of a beta-1,3-glucanase gene (Tag1) with anther-specific RNA and protein accumulation using antisense RNA inhibition. J Plant Physiol 160:1367–1373

    Article  CAS  PubMed  Google Scholar 

  • Chatterjee C, Nautiyal N (2000) Developmental aberrations in seeds of boron deficient sunflower and recovery. J Plant Nutr 23:835–841

    Article  CAS  Google Scholar 

  • Couée I, Sulmon C, Gouesbet G, Amrani AE (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459

    Article  PubMed  Google Scholar 

  • Cresti M, Keijzer CJ, Tiezzi A, Ciampolini F, Focardi S (1986) Stigma of Nicotiana: ultrastructural and biochemical studies. Am J Bot 73:1713–1722

    Article  CAS  Google Scholar 

  • Dafni A, Maués MM (1998) A rapid and simple procedure to determine stigma receptivity. Sex Plant Reprod 11:177–180

    Article  Google Scholar 

  • David A, Yadav S, Bhatla SC (2010) Sodium chloride stress induces nitric oxide accumulation in root tips and oil body surface accompanying slower oleosin degradation in sunflower seedlings. Physiol Plant 140:342–354

    Article  CAS  PubMed  Google Scholar 

  • Delp G, Palva ET (1999) A novel flower-specific Arabidopsis gene related to both pathogen-induced and developmentally regulated plant β-1,3-glucanase genes. Plant Mol Biol 39:565–575

    Article  CAS  PubMed  Google Scholar 

  • Dickinson HG (2000) Pollen stigma interactions so near yet so far. Trends Genet 16:373–376

    Article  CAS  PubMed  Google Scholar 

  • Dumas C (1977) Lipochemistry of the programic stage of a self-incompatible species: neutral lipids and fatty acids of the secretory stigma during its glandular activity, and of the solid style, the ovary and the anther in Forsythia intermedia Zab. (Heterostylic species). Planta 137:177–184

    Article  CAS  PubMed  Google Scholar 

  • Dumas C, Knox RB (1983) Callose and determination of pistil viability and incompatibility. Theor Appl Genet 67:1–10

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • García-Hernández ER, López GIC (2005) Structural cell wall proteins from five pollen species and their relationship with boron. Braz J Plant Physiol 17:375–381

    Article  Google Scholar 

  • Ghosh S, Shivanna KR (1984) Structure and cytochemistry of stigma and pollen-pistil interaction in Zephyranthes. Ann Bot 53:91–106

    Google Scholar 

  • Gomez L, Rubio E, Augé M (2002) A new procedure for extraction and measurement of soluble sugars in ligneous plants. J Sci Food Agric 82:360–369

    Article  CAS  Google Scholar 

  • Gupta UC (1998) Determination of boron, molybdenum and selenium in plant tissue. In: Kalra YP (ed) Handbook of reference methods for plant analysis. CRC Press, Florida, pp 172–174

    Google Scholar 

  • Gupta V, Mukhopadhyay A, Arumugam N, Sodhi YS, Pental D, Pradhan AK (2004) Molecular tagging of erucic acid trait in oilseed mustard (Brassica juncea) by QTL mapping and single nucleotide polymorphisms in FAE1 gene. Theor Appl Genet 108:743–749

    Article  CAS  PubMed  Google Scholar 

  • Halder NK, Farid ATM, Siddiky (2008) Effect of boron for correcting the deformed shape and size of Jackfruit. J Agric Rural Dev 6:37–42

  • Hara A, Radin NS (1978) Lipid extraction of tissues with a low-toxicity solvent. Anal Biochem 90:420–426

    Article  CAS  PubMed  Google Scholar 

  • Heslop-Harrison JS, Reger BJ (1986) Chloride and potassium ions and turgidity in the grass stigma. J Plant Physiol 124:55–60

    Article  CAS  Google Scholar 

  • Higashiyama T (2010) Peptide signaling in pollen-pistil interactions. Plant Cell Physiol 51:177–189

    Article  CAS  PubMed  Google Scholar 

  • Hiscock SJ, Allen AM (2008) Diverse cell signalling pathways regulate pollen–stigma interactions: the search for consensus. New Phytol 179:286–317

    Article  CAS  PubMed  Google Scholar 

  • Hiscock SJ, Hoedemaekers K, Friedman WE, Dickinson HG (2002a) The stigma surface and pollen–stigma interactions in Senecio squalidus L. (Asteraceae) following cross (compatible) and self (incompatible) pollinations. Int J Plant Sci 163:1–16

    Article  Google Scholar 

  • Hiscock SJ, Bown D, Gurr SJ, Dickinson HG (2002b) Serine esterases are required for pollen tube penetration of the stigma in Brassica. Sex Plant Reprod 15:65–74

    Article  CAS  Google Scholar 

  • Horneck DA, Hanson D (1998) Determination of potassium and sodium by flame emission spectrophotometry. In: Kalra YP (ed) Handbook of reference methods for plant analysis. CRC Press, Florida, pp 153–156

    Google Scholar 

  • Huang L, Bell RW, Dell B (2009) Exploring the physiological basis for high reproduction sensitivity to boron deficiency in plants. In: Proceedings of international plant nutrition ColloquiumXVI, Davis, California

  • Kalra G, Bhatla SC (1999) Distribution of membrane-bound calcium and activated calmodulin in cultured portoplasts of sunflower (Helianthus annuus L.). Curr Sci 76:1580–1584

    CAS  Google Scholar 

  • Kandasamy MK, Kristen U (1987) Developmental aspects of ultrastructure, histochemistry and receptivity of the stigma of Nicotiana sylvestris. Ann Bot 60:427–437

    Google Scholar 

  • Knox RB, Clarke A, Harrison S, Smith P, Marchalonis JJ (1976) Cell recognition in plants: determinants of the stigma surface and their pollen interactions. Proc Natl Acad Sci USA 73:2788–2792

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kräuter-Canham R, Bronner R, Steinmetz A (2001) SF21 is a protein which exhibits a dual nuclear and cytoplasmic localization in developing pistils of sunflower and tobacco. Ann Bot 87:241–249

    Article  Google Scholar 

  • Lavithis M, Bhalla PL (1995) Esterases in pollen and stigma of Brassica. Sex Plant Reprod 8:289–298

    Article  Google Scholar 

  • Lenartowska M, Rodríguez-García MI, Bednarska E (2001) Immunocytochemical localization of esterified and unesterified pectins in unpollinated and pollinated styles of Petunia hybrida Hort. Planta 213:182–191

    Article  CAS  PubMed  Google Scholar 

  • Lotan T, Ori N, Fluhr R (1989) Pathogenesis-related proteins are developmentally regulated in tobacco flowers. Plant Cell 1:881–887

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McConn M, Browse J (1996) The critical requirement of linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8:403–416

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McInnis SM, Desikan R, Hancock JT, Hiscock SJ (2006) Production of reactive oxygen species and reactive nitrogen species by angiosperm stigmas and pollen: potential signalling crosstalk? New Phytol 172:221–228

    Article  CAS  PubMed  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Morohashi Y, Matsushima H (2000) Development of beta-1,3-glucanase activity in germinated tomato seeds. J Exp Bot 51:1381–1387

    Article  CAS  PubMed  Google Scholar 

  • Ramasubbu R, Sreekala AK, Pandurangan AG (2010) Biochemical analysis of stigma of three endemic and endangered Impatiens L. J Biosci Res 1:13–16

    Google Scholar 

  • Rehman S, Yun SJ (2006) Developmental regulation of K accumulation in pollen, anthers, and papillae: are anther dehiscence, papillae hydration, and pollen swelling leading to pollination and fertilization in barley (Hordeum vulgare L.) regulated by changes in K concentration? J Exp Bot 57:1315–1321

    Article  CAS  PubMed  Google Scholar 

  • Rotisch T (1999) Source-sink regulation by sugar and stress. Curr Opin Plant Biol 2:198–206

    Article  Google Scholar 

  • Sage TL, Hristova-Sarkovski K, Koehl V, Lyew J, Pontieri V, Bernhardt P, Weston P, Bagha S, Chiu G (2009) Transmitting tissue architecture in basal-relictual angiosperms: implications for transmitting tissue origins. Am J Bot 96:183–206

    Article  PubMed  Google Scholar 

  • Sang YL, Xu M, Ma FF, Xu XH, Gao X-Q, Zhang XS (2012) Comparative proteomic analysis reveals similar and distinct features of proteins in dry and wet stigmas. Proteomics 12:1983–1998

    Article  CAS  PubMed  Google Scholar 

  • Schneiter AA, Miller JF (1981) Description of sunflower growth stages. Crop Sci 21:901–903

    Article  Google Scholar 

  • Shakya R, Bhatla SC (2010) A comparative analysis of the distribution and composition of lipidic constituents and associated enzymes in pollen and stigma of sunflower. Sex Plant Reprod 23:163–172

    Article  CAS  PubMed  Google Scholar 

  • Sharma B, Bhatla SC (2013a) Accumulation and scavenging of reactive oxygen species and nitric oxide correlate with stigma maturation and pollen–stigma interaction in sunflower. Acta Physiol Plant 35:2777–2787

    Article  CAS  Google Scholar 

  • Sharma B, Bhatla SC (2013b) Structural analysis of stigma development in relation with pollen–stigma interaction in sunflower. Flora 208:420–429

    Article  Google Scholar 

  • Silvério A, Mariath JEA (2010) The formation of the stigmatic surface in Passiflora elegans (Passifloraceae). Rudriguésia 61:569–574

    Google Scholar 

  • Teixeira SP, Capucho LC, Machado SR (2011) Two novel reports of semidry stigmatic surface in Asteraceae. Flora 206:328–333

    Article  Google Scholar 

  • Trevelyan WE, Harrison JS (1952) Studies on yeast metabolism. I. Fractionation and microdetermination of cell carbohydrates. Biochem J 50:298–303

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tucker MR, Paech NA, Willemse MTM, Koltunow AMG (2001) Dynamics of callose deposition and β-1,3-glucanase expression during reproductive events in sexual and apomictic Hieracium. Planta 212:487–498

    Article  CAS  PubMed  Google Scholar 

  • Wakelin AM, Leung DWM (2009) β-1,3-Glucanase activity in the stigma of healthy petunia flowers. Biol Plant 51:69–74

    Article  Google Scholar 

  • Watson ME (1998) Boron. In: Brown JR (ed) Recommended chemical soil test procedures for the north central region. Missouri agricultural experiment station SB 1001, Columbia, pp 445–448

  • Willats WG, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27

    Article  CAS  PubMed  Google Scholar 

  • Wolters-Arts M, Lush WM, Mariani C (1998) Lipids are required for directional pollen-tube growth. Nature 392:818–821

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Digital imaging work was undertaken on the photomicroscope provided by Alexander von Humboldt Foundation (Germany) to SCB. Thanks are due to Dr. Rashmi Shakya for help in various ways. GC was carried out with help of Dr. Y.S. Sodhi, Center for Genetic Manipulation of Crop plants, Delhi. This work was supported by University Grants Commission (UGC) and MM (PG) College, Modinagar in the form of teacher research fellowship to BS.

Author information

Authors and Affiliations

  1. Laboratory of Plant Physiology and Biochemistry, Department of Botany, University of Delhi, North Campus, Delhi, 110007, India

    Basudha Sharma & S. C. Bhatla

Authors
  1. Basudha Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. C. Bhatla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. C. Bhatla.

Additional information

Communicated by J. V. Huylenbroeck.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sharma, B., Bhatla, S.C. Elemental and biochemical markers of stigma receptivity in sunflower. Acta Physiol Plant 36, 1299–1311 (2014). https://doi.org/10.1007/s11738-014-1504-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-014-1504-1

Keywords

Search

Navigation