Stigma receptivity with pollen in sunflower accompanies novel histochemical and biochemical changes in both male and female reproductive structures

Research Articles | Published:

Print ISSN : 0970-4078.
Online ISSN : 2229-4473.
Website:www.vegetosindia.org
Pub Email: contact@vegetosindia.org
Doi: 10.1007/s42535-020-00118-5
First Page: 376
Last Page: 384
Views: 634


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.


Glycoproteins, Peroxidases, Proteases, Tryphine, Pollen–pistil interaction, Sunflower


*Pdf Download

(*Only SPR Members can download pdf file; #Open Access;)

References

  1. Aelst ACV, Went JLV (1992) Ultrastructural and immuno-localization of pectins and glycoproteins in Arabidopsis thaliana pollen grains. Protoplasma 168:14–19

  2. 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

  3. 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

  4. 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

  5. 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

  6. 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

  7. Bredemeijer GMM (1982) Pollen peroxidases. J Palynol 18:1–11

  8. Bredemeijer GMM (1984) The role of peroxidases in pistil–pollen interactions. Theor Appl Genet 68:193–206

  9. 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

  10. 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

  11. 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

  12. 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

  13. de Graff BHJ, Derksen JWM, Mariani C (2001) Pollen and pistil in the progamic phase. Sex Plant Reprod 14:41–55

  14. 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

  15. Heslop-Harrison Y (2000) Control gates and micro-ecology: the pollen–stigma interaction in perspective. Ann Bot 85:5–13

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

  17. 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

  18. 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

  19. 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

  20. 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

  21. 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

  22. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

  23. 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

  24. 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

  25. 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

  26. Lyon H (1991) Theory and strategy in histochemistry: a guide to the selection and understanding of techniques. Springer-Verlag, Berlin

  27. 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

  28. 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

  29. Radlowski M (2005) Proteolytic enzymes from generative organs of flowering plants (Angiospermae). J Appl Genet 46:247–257

  30. Radlowski M, Kalinowski A, Królikowski Z, Bartkowiak S (1994a) Protease activity from maize pollen. Phytochemistry 35:853–856

  31. 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

  32. Radlowski M, Kalinowski A, Adamczyk J, Królikowski Z, Bartkowiak S (1996) Proteolytic activity in the maize pollen wall. Physiol Plant 98:172–178

  33. 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

  34. Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press, New York

  35. Shakya R (2008) Structural and biochemical analysis of pollen–stigma interaction in sunflower. Ph.D. thesis, Department of Botany, University of Delhi, India

  36. 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

  37. 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

  38. 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

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

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

  41. Shivanna KR (2003) Pollen biology and biotechnology. Oxford Press, New Delhi

  42. 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

  43. Swanson R, Edlund AF, Preuss D (2004) Species specificity in pollen–pistil interactions. Annu Rev Genet 38:793–818

  44. 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

  45. 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

  46. 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


    47.  


Acknowledgements

The author thanks Council of Scientific and Industrial Research for financial support and is grateful to Professor S C Bhatla, Department of Botany, University of Delhi for providing laboratory facilities for this work.


Author Information

Shakya Rashmi
Department of Botany, Miranda House, University of Delhi, Delhi, India
rashmi.shakya@mirandahouse.ac.