Evaluation of stigma receptivity and its properties in Helianthus annuus L. (Asteraceae)

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Research Articles | Published:

Print ISSN : 0970-4078.
Online ISSN : 2229-4473.
Pub Email: contact@vegetosindia.org
Doi: 10.1007/s42535-022-00419-x
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Keywords: Antimicrobial, Esterases, Flavonoids, Peroxidases, Stigma


Stigma receptivity has a critical role in the development of flowering plants. The time of stigma receptivity is important as it results in pollen recognition, adhesion and formation of pollen tube. The duration of receptivity may vary from few hours to few days. At receptivity, the stigma accumulates different biomolecules required for reproductive success. The purpose of present investigation is to identify the biomolecules and assess their critical role, in receptivity of stigma. Receptivity of Helianthus annuus L. (family Asteraceae), is evaluated by activity of enzymatic markers (through enzymatic method for histochemical localization), and the associated signaling molecules (localized by confocal microscopy). Esterases and Peroxidases act as the marker enzymes for receptivity in flowering plants. Interplay of reactive oxygen species (ROS), hydrogen peroxides and flavonoids facilitate stigma to override the stressful environmental conditions and also provide it resistance against pathogens. Present investigations, further reveal that the secondary metabolites present in stigma of sunflower act efficiently against the gram negative (Escherichia coli) and gram positive (Staphylococcus spp.) bacteria thereby highlighting stigma’s ability to defend itself and inflorescence as a whole, from microbial infection during its development. The study, thus highlights the interplay of enzymes, reactive oxygen species and flavonoids in increasing cross-tolerance in stigma of H. annuus.

Antimicrobial, Esterases, Flavonoids, Peroxidases, Stigma


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

Baroncelli S, Lercari B, Cecconi F, Pugliesi C (1990) Light control of elongation of filament in sunflower (Helianthus annuus L.). Photochem Photobiol 52:229–231

Bednarska E, Lenartowska M, Niekraś L (2005) Localization of pectins and Ca2+ ions in unpollinated and pollinated wet (Petunia hybrida Hort.) and dry (Haemanthus albiflos L.) stigma. Folia Histochem Cytobiol 43:249–259

Beltramo C, Marinoni DT, Perrone I, Botta R (2012) Isolation of a gene encoding for a class III peroxidase in female flower of Corylus avellana L. Mol Biol Rep 39:4997–5008

Beneš K (1968) On the stainability of plant cell walls with alcian blue. Biol Plant 10:334–346

Bhatla SC, Gogna M, Jain P, Singh N, Mukherjee S, Kalra G (2021) Signaling mechanisms and biochemical pathways regulating pollen-stigma interaction, seed development and seedling growth in sunflower under salt stress. Plant Signal Behav 16(11):1958129. https://doi.org/10.1080/15592324.2021.1958129

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

Brunetti C, Ferdinando MD, Fini A, Pollastri S, Tattini M (2013) Flavonoids as antioxidants and developmental regulators: relative significance in plants and humans. Int J Mol Sci 14:3540–3555

Chen J, Gutjahr C, Bleckmann A, Dresselhaus T (2015) Calcium signaling during reproduction and biotrophic fungal interactions in plants. Mol Plant 8(4):595–611

Chen Z, Raji M (2020) Role of reactive oxygen species in modulating cross tolerance in plants via flavonoids. In: Hossain MA, Liu F, Burritt DJ, Fujita M, Huang M (eds) Priming-mediated stress and cross-stress tolerance in crop plants. Academic Press, ISBN 9780128178928

Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. J Exp Bot 60:391–408

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

de Graff BHJ, Derksen JWM, Mariani C (2001) Pollen and pistil in the programic phase. Sexual Plant Reprod 14:411–455

Dickinson H (1995) Dry stigmas, water and self-incompatibility in Brassica. Sexual Plant Reprod 8:1–10

Dudek B, Warskulat AC, Schneider B (2016) The occurrence of flavonoids and related compounds in flower sections of Papaver nudicaule. Plants (basel) 5(2):28. https://doi.org/10.3390/plants5020028

Fábián A, Sáfrán E, Szabó-Eitel G, Barnabás B, Jäger K (2019) Stigma functionality and fertility are reduced by heat and drought co-stress in wheat. Front Plant Sci 10:244

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

Galen C, Plowright RC (1987) Testing the accuracy of using peroxidase activity to indicate stigma receptivity. Can J Bot 65:107–111

Ghosh S, Shivanna KR (1980) Pollen-pistil interaction in Linum grandiflorum: stigma-surface proteins and stigma receptivity. Proc Indian Natl Sci Acad B46:177–183

Gonelimali FD, Lin J, Miao W, Xuan J, Charles F, Chen M, Hatab SR (2018) Antimicrobial properties and mechanism of action of some plant extracts against food pathogens and spoilage microorganisms. Front Microbiol 9:1639

Górniak I, Bartoszewski R, Króliczewski J (2019) Comprehensive review of antimicrobial activities of plant flavonoids. Phytochem Rev 18:241–272

Heslop-Harrison Y, Shivanna KR (1977) The receptive surface of angiosperm. Ann Bot 41:1233–1258

Hiscock SJ, Hoedemaekers K, Friedman WE, Dickinson HG (2002) 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

Hong L, Shen H, Ye W, Cao H, Wang Z (2008) Secondary pollen presentation and style morphology in the invasive weed Mikania micrantha in South China. Bot Stud 49:253–260

Howell GJ, Slater AT, Knox RB (1993) Secondary pollen presentation in angiosperms and its biological significance. Aust J Bot 41:417–438

Hsieh K, Huang AH (2007) Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum-derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell 19:582–596

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

Koning RE (1983) The roles of plant hormones in style and stigma growth in Gaillardia grandiflora (Asteraceae). Amer J Bot 70:978–986

Kulloli SK, Ramasubbu R, Sreekala AK, Pandurangan AG (2010) Cytochemical localization of stigma-surface esterases in three species of Impatiens (Balsaminaceae) of western ghats. Asian J Exp Biol Sci 1:106–111

Mattsson O, Knox RB, Heslop-Harrison J, Heslop-Harrison Y (1974) Protein pellicle of stigmatic papillae as a probable recognition site in incompatibility reactions. Nature 247:298–300

McInnis SM, Costa LM, Gutiérrez-Marcos JF, Henderson CA, Hiscock SJ (2005) Isolation and characterization of a polymorphic stigma-specific class III peroxidase gene from Senecio squalidus L. (Asteraceae). Plant Mol Biol 57:659–677

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

McInnis SM, Emery DC, Porter R, Desikan R, Hancock JT, Hiscock SJ (2006b) The role of stigma peroxidases in flowering plants: insights from further characterization of stigma-specific peroxidase (SSP) from Senecio squalidus (Asteraceae). J Exp Bot 57:1835–1846

Onus AN (2000) Structure of the stigma and style in Capsicum eximium and the effects of pollination. Turk J Bot 24:337–346

Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9:534–540

Perez IB, Brown PJ (2014) The role of ROS signaling in cross-tolerance: from model to crop. Front Plant Sci 5:754

Polveiro RC, Vidigal PMP, Mendes TAO et al (2020) Effects of enrofloxacin treatment on the bacterial microbiota of milk from goats with persistent mastitis. Sci Rep 10:4421

Pruski JF, Sancho G (2004) Asteraceae or Compositae (Aster or Sunflower Family). In: Smith N et al (eds) Flowering plants of the neotropics. Princeton Univ. Press, Princeton

Quinn PJ, Carter ME, Markey B, Carter GR (1994) Clinical veterinary microbiology. Wolf/Mosby, London

Reger BJ (1989) Stigma surface secretions of Pennisetum americanum. Amer J Bot 76:1–5

Sammataro D, Garment MB, Erickson Jr EH (1985) Anatomical features of the sunflower floret. Helia (FAO, Romania) 25–31

Sanchez AM, Bosch M, Bots M, Nieuwland J, Feron R, Mariani C (2004) Pistil factors controlling pollination. Plant Cell 16:S98–S106

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

Shakya R (2020) Stigma receptivity with pollen in sunflower accompanies novel histochemical and biochemical changes in both male and female reproductive structures. Vegetos 33:376–384. https://doi.org/10.1007/s42535-020-00118-5

Sharma B (2019) An analyses of flavonoids present in the inflorescence of sunflower. Braz J Bot 42:421–429

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 Planta 35:2777–2787

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

Sharma B, Bhatla SC (2014) Elemental and biochemical markers of stigma receptivity in sunflower. Acta Physiol Planta 36:1299–1311

Sharma B, Shakya R, Bhatla SC (2014) Floral biology of Sunflowers: a histological and physiological analysis. In: Arribas J (ed) Growth and development, environmental influences and pests/diseases. Nova, New York, pp 19–42

Shivanna KR, Rangaswamy NS (1992) Pollen biology: a laboratory manual. Springer-Verlag, Berlin

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

Torres C, Galetto L (2007) Style morphological diversity of some Asteraceae species from Argentina: systematic and functional implications. J Plant Res 120(3):359–364

Verma H, Rawat S, Sharma N, Jaiswal V, Singh RB (2018) Prevalence, bacterial etiology and antibiotic susceptibility pattern of bovine mastitis in Meerut. J Entomol Zool Stud 6:706–709

Wu H-C, Bulgakov VP, Jinn T-L (2018) Pectin methylesterases: cell wall remodeling proteins are required for plant response to heat stress. Front Plant Sci 9:1612. https://doi.org/10.3389/fpls.2018.01612

Xingguo L, Jia Y, Kumar A, Yuzhe N, Xiaoyu L, Yuhua L, Marcus AS (2017) Flavonoids and ROS play opposing roles in mediating pollination in ornamental Kale (Brassica oleracea var. acephala). Mol Plant 10:1361–1364

Zhang MJ, Zhang XS, Gao XQ (2020) ROS in the male–female interactions during pollination: function and regulation. Front Plant Sci 11:177



The corresponding author is grateful to Multanimal Modi college for providing basic research facilities. The authors express gratitude for the assistance received from the Laboratory of Plant Physiology and Biochemistry (C/o Prof. SC Bhatla), University of Delhi for imaging facility.

Author Information

Sharma B.
Department of Botany, Multanimal Modi College, Modinagar, India
Kalra G.
Department of Botany, Acharya Narendra Dev College, University of Delhi, Delhi, India

Verma H.
Department of Veterinary and Animal Sciences, Sardar Vallabhbhai Patel University of Agriculture and Technology, Meerut, India