Stigma receptivity with pollen in sunflower accompanies novel histochemical and biochemical changes in both male and female reproductive structures
Shakya Rashmi
Research Articles | Published: 11 April, 2020
DOI: 10.1007/s42535-020-00118-5
First Page: 376
Last Page: 384
Views: 3311
Keywords: Glycoproteins, Peroxidases, Proteases, Tryphine, Pollen–pistil interaction, Sunflower
Abstract
Pollen–pistil interaction is one of the widely studied cell–cell communication events in angiosperms. Pollination of the receptive pistil with compatible pollen and the subsequent steps that determines the success of fertilization depend on the cooperative events between pollen and pistil. Before the onset of these interactive events between pollen and pistil, both the participants prepare themselves for the upcoming complex cellular events. Receptive surface of stigma is characterized by the accumulation of reactive oxygen species and expression of specific biomolecules and enzymes, such as non-specific esterases and peroxidases. Pollen grains produce nitric oxide that scavenge reactive oxygen species generated on stigma surface after pollination and just prior to pollen germination. Present work reports accumulation of glycoproteins, lipids and phospholipids at the base of stigmatic papillae in mature receptive stigma. A 31 kDa glycoprotein has been detected in stigma homogenate. Stigma exhibit enhanced expression of peroxidase isoforms relative to buffer soluble fractions of pollen, i.e. intact pollen, internal pollen and tryphine fractions. A 54 kDa protease is expressed in pollen grains as well as stigma. Biochemical analyses of these biomolecules in pollen and stigma relative to other vegetative (corolla of ray and disc floret, bracts, young leaves) and reproductive (anther wall and ovary) parts highlight the implications of these biomolecules in pollen–stigma interaction.
References
- Aelst ACV, Went JLV (1992) Ultrastructural and immuno-localization of pectins and glycoproteins in Arabidopsis thaliana pollen grains. Protoplasma 168:14–19
- Alba CM, de Forchetti SM, Quesada MA, Valpuesta V, Tigier HA (1998) Localization and general properties of developing peach seed coat and endosperm peroxidase isoenzyme. Plant Growth Regul 17:7–11
- Allen AM, Thorogood CJ, Hegarty MJ, Lexer C, Hiscock SJ (2011) Pollen–pistil interactions and self-incompatibility in the Asteraceae: new insights from studies of Senecio squalidus (Oxford ragwort). Ann bot 108:687–698
- Bagarozzi DA, Pike R, Potempa J, Travis J (1996) Purification and characterization of a novel endopeptidase in ragweed (Ambrosia artemisiifolia) pollen. J Biol Chem 271:26227–26232
- Bagarozzi DA, Potempa J, Travis J (1998) Purification and characterization of an arginine-specific peptidase from ragweed (Ambrosia artemisiifolia) pollen. Am J Respir Cell Mol Biol 18:363–369
- Bredemeijer GMM, Blaas J (1975) A possible role of a stylar peroxidase gradient in the rejection of incompatible growing pollen tubes. Acta Bot Neerl 24:37–48
- Bredemeijer GMM (1982) Pollen peroxidases. J Palynol 18:1–11
- Bredemeijer GMM (1984) The role of peroxidases in pistil–pollen interactions. Theor Appl Genet 68:193–206
- Chen F, Foolad MR (1997) Molecular organization of a gene in barley which encodes a protein similar to aspartic protease and its specific expression in nucellar cells during degeneration. Plant Mol Biol 35:821–831
- Doughty J, Hdderson F, Mc Cubbin A, Dickinson H (1993) Interaction between a coating borne peptide of the Brassica pollen grain and stigmatic S (self-incompatibility)-locus-specific glycoprotein. Proc Natl Acad Sci USA 90:467–471
- Dubray G, Bezard G (1982) A highly sensitive periodic acid-silver stain for 1, 2-dio groups of glycoproteins and polysaccharides in polyacrylamide gels. Anal Biochem 119:325–329
- Edlund AF, Swanson R, Preuss D (2004) Pollen and stigma structure and function: the role of diversity in pollination. Plant Cell 16(Suppl):S84–S97
- de Graff BHJ, Derksen JWM, Mariani C (2001) Pollen and pistil in the progamic phase. Sex Plant Reprod 14:41–55
- Grobe K, Becker WM, Schlaak M, Petersen A (1999) Grass group I allergens (β-expansins) are novel, papain-related proteinases. Eur J Biochem 263:33–40
- Heslop-Harrison Y (2000) Control gates and micro-ecology: the pollen–stigma interaction in perspective. Ann Bot 85:5–13
- Heslop-Harrison Y, Shivanna KR (1977) The receptive surface of the angiosperm stigma. Ann Bot 41:1233–1258
- Heimgartner U, Pietrzak M, Geertsen R, Brodelius P, da Silva Figueiredo AC, Pais MSS (1990) Purification and partial characterization of milk clotting proteases from flowers of Cynara cardunculus. Phytochemistry 29:1405–1410
- Heussen C, Dowdle EB (1980) Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Anal Biochem 102:196–202
- Hiscock SJ, Doughty J, Willis AC, Dickinson HG (1995) A 7-kDa pollen coating-borne peptide from Brassica napus interacts with S-locus glycoproteins and S-locus-related glycoprotein. Planta 196:367–374
- Kandasamy MK, Paolillo DJ, Faraday CD, Nasrallah JB, Nasrallah ME (1989) The S-locus specific glycoproteins of Brassica accumulate in the cell wall of developing stigma papillae. Dev Biol 134:462–472
- Kimura Y, Maeda M, Kimura M, Lai OM, Tan SH, Hon SM, Chew FT (2002) Purification and characterization of a 31-kDa palm pollen glycoprotein (Ela g Bd 31 K), which is recognized by IgE from palm pollinosis patients. Biosci Biotechnol Biochem 66:820–827
- Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
- Lewis D, Burrage S, Walls D (1967) Immunological reactions of single pollen grains, electrophoresis and enzymology of pollen protein exudates. J Exp Bot 18:371–378
- Luu DT, Heizmann P, Dumas C (1997) Pollen–stigma adhesion in kale is not dependent on the self- (in) compatibility genotype. Plant Physiol 115:1221–1230
- Luu DT, Marty-Mazars D, Trick M, Dumas C, Heizmann P (1999) Pollen–stigma adhesion in Brassica spp. involves SLG and SLR1 glycoproteins. Plant Cell 11:251–262
- Lyon H (1991) Theory and strategy in histochemistry: a guide to the selection and understanding of techniques. Springer-Verlag, Berlin
- McInnis SM, Emery DC, Porter R, Desikan R, Hancock JT, Hiscock SJ (2006) The role of stigma peroxidases in flowering plants: insights from further characterization of a stigma-specific peroxidase (SSP) from Senecio squalifus (Asteraceae). J Exp Bot 57:1846–1853
- Poddubnaya-Arnoldi VA, Zinger NV, Petrovskaja TP, Polunina NN (1961) Histochemical study of the pollen grains and pollen tubes in the angiosperms. Rec Adv Bot 1:682–685
- Radlowski M (2005) Proteolytic enzymes from generative organs of flowering plants (Angiospermae). J Appl Genet 46:247–257
- Radlowski M, Kalinowski A, Królikowski Z, Bartkowiak S (1994a) Protease activity from maize pollen. Phytochemistry 35:853–856
- Radlowski M, Kalinowski A, Siedlewska A, Adamczyk J, Królikowski Z, Bartkowiak S (1994b) The regulating activity of native protease in maize pollen grains. Flower Newsl 17:49–52
- Radlowski M, Kalinowski A, Adamczyk J, Królikowski Z, Bartkowiak S (1996) Proteolytic activity in the maize pollen wall. Physiol Plant 98:172–178
- Ramalho-Santos M, Pissarra J, Verissimo P, Pereira S, Salema R, Pires E, Faro CJ (1997) Cardosin A, an abundant aspartic proteinase, accumulates in protein storage vacuoles in the stigmatic papillae of Cynara cardunculus L. Planta 203:204–212
- Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press, New York
- Shakya R (2008) Structural and biochemical analysis of pollen–stigma interaction in sunflower. Ph.D. thesis, Department of Botany, University of Delhi, India
- 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
- Shakya R, Bhatla SC (2018) Pollination, fertilization and seed development. In: Bhatla SC, Lal MA (eds) Plant physiology, development and metabolism. Springer, Singapore, pp 821–856
- 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
- Sharma B, Bhatla SC (2013b) Structural analysis of stigma development in relation with pollen–stigma interaction in sunflower. Flora 208:420–429
- Sharma B (2019) An analyses of flavonoids present in the inflorescence of sunflower. Braz J Bot 42:421–429
- Shivanna KR (2003) Pollen biology and biotechnology. Oxford Press, New Delhi
- Suarez-Cervera M, Asturias JA, Vega-Maray A, Castells T, Lopez-Iglesias C, Ibarolla I, Arilla MC, Gabarayeva N, Seoane-Camba J (2005) The role of allergenic proteins Pla a 1 and Pla a 2 in the germination of Platanus acerifolia pollen grains. Sex Plant Reprod 18:101–112
- Swanson R, Edlund AF, Preuss D (2004) Species specificity in pollen–pistil interactions. Annu Rev Genet 38:793–818
- Takayama S, Shiba H, Iwano M, Asano K, Hara M (2000) Isolation and characterization of pollen coat proteins of Brassica campestris that interact with S locus-related glycoprotein 1 involved in pollen–stigma adhesion. Proc Natl Acad Sci USA 97:3765–3770
- Umbach AL, Lalonde BA, Kandasamy MK, Nasrallah JB, Nasrallah ME (1990) Immunodetection of protein glycoforms encoded by 2 independent genes of the self-incompatibility multigene family of Brassica. Plant Physiol 93:739–747
- Verissimo P, Faro C, Moir AJG, Lin Y, Tang J, Pires E (1996) Purification, characterization and partial amino acid sequencing of two new aspartic proteinases from fresh flowers of Cynara cardunculus L. Eur J Biochem 235:762–768
Author Information
Department of Botany, Miranda House, University of Delhi, Delhi, India