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Callose is integral to the development of permanent tetrads in the liverwort Sphaerocarpos

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Abstract

A striking feature of the liverwort Sphaerocarpos is that pairs of male and female spores remain united in permanent tetrads. To identify the nature of this phenomenon and to test the hypothesis that callose is involved, we examined spore wall development in Sphaerocarpos miche lii, with emphasis on the appearance, location and fate of callose vis-à-vis construction of the sculptoderm. All stages of sporogenesis were examined using differential interference contrast optics, and aniline blue fluorescence to locate callose. For precise localization, specimens were immunogold labeled with anti-callose antibody and observed in the transmission electron microscope. Callose plays a role in Sphaerocarpos spore wall development not described in any other plant, including other liverworts. A massive callose matrix forms outside of the sculptured sporocyte plasmalemma that predicts spore wall ornamentation. Consequently, layers of exine form across adjacent spores uniting them. Spore wall development occurs entirely within the callose and involves the production of six layers of prolamellae that give rise to single or stacked tripartite lamellae (TPL). Between spores, an anastomosing network of exine layers forms in lieu of intersporal septum development. As sporopollenin assembles on TPL, callose progressively disappears from the inside outward leaving layers of sporopollenin impregnated exine, the sculptoderm, overlying a thick fibrillar intine. This developmental mechanism provides a direct pathway from callose deposition to sculptured exine that does not involve the intermediary primexine found in pollen wall development. The resulting tetrad, encased in a single wall, provides a simple model for development of permanent dyads and tetrads in the earliest fossil plants.

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Abbreviations

MLL:

Multilamellate layer

TPL:

Tripartite lamellae

References

  • Allen CE (1917) A chromosome difference correlated with sex differences in Sphaerocarpos. Science 46:466–467

    Article  CAS  PubMed  Google Scholar 

  • Allen CE (1919) The basis of sex inheritance in Sphærocarpos. Proc Am Philos Soc 58:289–316

    Google Scholar 

  • Allen CE (1924) Gametophytic inheritance in Sphaerocarpos I. Intraclonal variation, and the inheritance of the tufted character. Genetics 9:530–587

    PubMed Central  CAS  PubMed  Google Scholar 

  • Allen CE (1925) The inheritance of a pair of sporophytic characters in Sphaerocarpos. Genetics 10:72–79

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ariizumi T, Toriyama K (2011) Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol 62:437–460

    Article  CAS  PubMed  Google Scholar 

  • Ariizumi T, Hatakeyama K, Hinata K, Inatsugi R, Nishida I, Sato S, Kato T, Tabata S, Toriyama K (2004) Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana. Plant J 39:170–181

    Article  CAS  PubMed  Google Scholar 

  • Brown RC, Lemmon BE (1987) Involvement of callose in determination of exine patterning in three hepatics of the subclass Jungermanniidae. Mem NY Botan G 45:111–121

    Google Scholar 

  • Brown RC, Lemmon BE (1990) Sporogenesis in bryophytes. In: Blackmore SB, Knox RB (eds) Microspores: evolution and ontogeny. Academic Press, London, pp 55–94

    Chapter  Google Scholar 

  • Brown RC, Lemmon BE (1993) Spore wall development in the liverwort Fossombronia wondraczekii (Corda) Dum. J Hattori Bot Lab 74:83–94

    Google Scholar 

  • Brown RC, Lemmon BE (2013) Sporogenesis in bryophytes: patterns and diversity in meiosis. Bot Rev. doi:10.1007/s12229-012-9115-2

  • Brown RC, Lemmon BE, Renzaglia KS (1986) Sporocytic control of spore wall pattern in liverworts. Am J Bot 73:593–596

    Article  Google Scholar 

  • Chang HS, Zhang C, Chang YH, Zhu J, Xu XF, Shi ZH, Zhang XL, Xu L, Huang H, Zhang S, Yang ZN (2012) No primexine and plasma membrane undulation is essential for primexine deposition and plasma membrane undulation during microsporogenesis in Arabidopsis. Plant Physiol 158:264–272

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dong X, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DPS (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J 42:315–328

    Article  CAS  PubMed  Google Scholar 

  • Doyle WT (1975) Spores of Sphaerocarpos donnellii. Bryologist 78:80–84

    Article  Google Scholar 

  • Dubois-Tylski T (1981) Utilisation de fluorochromes pour l’observation des parois cellulaires chez trois especes de Closterium (Desmidiales) au cours de leur reproduction sexuee. Cryptogam Algol 1:277–287

    Google Scholar 

  • Edwards D, Morris JL, Richardson JB, Kenrick P (2014) Cryptospores and cryptophytes reveal hidden diversity in early land floras. New Phytol 202:50–78

    Article  PubMed  Google Scholar 

  • Enns LC, Kanaoka MM, Torii KU, Comai L, Okada K, Cleland RE (2005) Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility. Plant Mol Biol 58:333–349

    Article  CAS  PubMed  Google Scholar 

  • Francis KE, Lam SY, Copenhaver GP (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiol 142:1004–1013

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gabarayeva N, Hemsley AR (2006) Merging concepts: the role of self-assembly in the development of pollen wall structure. Rev Palaeobot Palynol 138:121–139

    Article  Google Scholar 

  • Graham LE (1993) Origin of land plants. Wiley, New York

    Google Scholar 

  • Graham LE, Taylor C III (1986) Occurrence and phylogenetic significance of “special walls” at meiosporogenesis in Coleochaete. Am J Bot 73:597–601

    Article  Google Scholar 

  • Gray J (1985) The microfossil record of early land plants: advances in understanding of early terrestrialization, 1970–1984. Philos Trans Roy Soc B 309:167–192

    Article  Google Scholar 

  • Guan YF, Huang XY, Zhu J, Gao JF, Zhang HX, Yang ZN (2008) RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiol 147:852–863

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Izhar S, Frankel R (1971) Mechanism of male sterility in Petunia: the relationship between pH, callase activity in the anthers, and the breakdown of the microsporogenesis. Theor Appl Genet 41:104–108

    Article  CAS  PubMed  Google Scholar 

  • Lugardon B (1990) Pteridophyte sporogenesis: a survey of spore wall ontogeny and fine structure in a polyphyletic plant group. In: Blackmore S, Knox RB (eds) Microspores: evolution and ontogeny. Academic Press, London, pp 95–120

    Chapter  Google Scholar 

  • McLetchie DN (1992) Sex ratio from germination through maturity and its reproductive consequences in the liverwort Sphaerocarpos texanus. Oecologia 92:273–278

    Article  Google Scholar 

  • McLetchie DN, Collins AL (2001) Identification of DNA regions specific to the X and Y chromosomes in Sphaerocarpos texanus. Bryologist 104:543–547

    Article  CAS  Google Scholar 

  • Morbelli MA, Lugardon B (2012) Microspore wall organisation and ultrastructure in two species of Selaginella (Lycophyta) producing permanent tetrads. Grana 51:97–106

    Article  Google Scholar 

  • Nishikawa S-I, Zinkl GM, Swanson RJ, Maruyama D, Preuss D (2005) Callose (β-1, 3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth. BMC Plant Biol 5:22

    Article  PubMed Central  PubMed  Google Scholar 

  • Paxson-Sowders DM, Owen HA, Makaroff CA (1997) A comparative ultrastructural analysis of exine pattern development in wild-type Arabidopsis and a mutant defective in pattern formation. Protoplasma 198:53–65

    Article  Google Scholar 

  • Paxson-Sowders DM, Dodrill CH, Owen HA, Makaroff CA (2001) DEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis. Plant Physiol 127:1739–1749

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Petounnikow A (1867) Sur les organs reproduceors du Sphaerocarpus terrestris. B Soc Bot Fr 14:137–142

    Article  Google Scholar 

  • Renzaglia KS, Schuette S, Duff J, Ligrone R, Shaw AJ, Mishler BD, Duckett JG (2007) Bryophyte phylogeny: advancing the molecular and morphological frontiers. Bryologist 110:179–213

    Article  Google Scholar 

  • Rhee SY, Somerville CR (1998) Tetrad pollen formation in quartet mutants of Arabidopsis thaliana is associated with persistence of pectic polysaccharides of the pollen mother cell wall. Plant J 15:79–88

    Article  CAS  PubMed  Google Scholar 

  • Rhee SY, Osborne E, Poindexter PD, Somerville CR (2003) Microspore separation in the quartet3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant Physiol 133:1170–1180

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Scherp P, Grotha R, Kutschera U (2001) Occurrence and phylogenetic significance of cytokinesis-related callose in green algae, bryophytes, ferns and seed plants. Plant Cell Rep 20:143–149

    Article  CAS  Google Scholar 

  • Schuette S (2012) Ultrastructure, immunocytochemistry, and bioinformatics of spore development in the moss Physcomitrella and the hornwort Dendroceros. Dissertation, Southern Illinois University, Carbondale

  • Schuette S, Johnson E (2010) Sphaerocarpos michelii Bellardi (Sphaerocarpaceae) new in Illinois. Evansia 27:34–35

    Article  Google Scholar 

  • Schuette S, Wood AJ, Geisler M, Geisler-Lee J, Ligrone R, Renzaglia KS (2009) Novel localization of callose in the spores of Physcomitrella patens and phylogenomics of the callose synthase gene family. Ann Bot Lond 103:749–756

    Article  CAS  Google Scholar 

  • Sørensen I, Pettolino FA, Bacic A, Ralph J, Fachuang L, O’Neill MA, Fei Z, Rose JKC, Domozych DS, Willats WGT (2011) The charophycean green algae provide insights into the early origins of plant cell walls. Plant J 68:201–211

    Article  PubMed  Google Scholar 

  • Suzuki T, Masaoka K, Nishi M, Nakamura K, Ishiguro S (2008) Identification of kaonashi mutants showing abnormal pollen exine structure in Arabidopsis thaliana. Plant Cell Physiol 49:1465–1477

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Taylor WA (1995a) Ultrastructure of Tetrahedraletes medinensis (Strother and Traverse) Wellman and Richardson, from the upper Ordovician of southern Ohio. Rev Paleobot Palyno 85:183–187

    Article  Google Scholar 

  • Taylor WA (1995b) Spores in earliest land plants. Nature 373:391–392

    Article  CAS  Google Scholar 

  • Taylor ML, Hudson PJ, Rigg JM, Strandquist JN, Green JS, Thiemann TC, Osborn JM (2013) Pollen ontogeny in Victoria (Nymphaeales). J Plant Sci 174:1259–1276

    Article  Google Scholar 

  • Wallace S, Fleming A, Wellman CH, Beerling DJ (2011) Evolutionary development of the plant spore and pollen wall. AoB Plants. doi:10.1093/aobpla/plr027

  • Wellman CH (2004) Origin, function and development of the spore wall in early land plants. In: Hemsley A, Poole I (eds) The evolution of plant physiology. Elsevier, Oxford, pp 43–63

    Chapter  Google Scholar 

  • Wellman CH, Osterloff P, Mohluddin U (2003) Fragments of the earliest land plants. Nature 425:282–283

    Article  CAS  PubMed  Google Scholar 

  • Winiarczyk K, Jaroszuk-Ściseł J, Kupisz K (2012) Characterization of callase (β-1, 3-d-glucanase) activity during microsporogenesis in the sterile anthers of Allium sativum L. and the fertile anthers of A. atropurpureum. Sex Plant Reprod 25:123–131

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Andres Womac, Amelia Merced, Scott Schuette, and Bryan Piatkowski for technical assistance. This work was supported by NSF grants EF 0531751 and DGE 0638722.

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Authors and Affiliations

  1. Department of Plant Biology, MC: 6509, Southern Illinois University Carbondale, Carbondale, IL, 62901, USA

    Karen S. Renzaglia & Renee A. Lopez

  2. Department of Biology, Virginia Wesleyan College, 1584 Wesleyan Drive, Norfolk, VA, 23502, USA

    Eric E. Johnson

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  1. Karen S. Renzaglia
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  2. Renee A. Lopez
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  3. Eric E. Johnson
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Correspondence to Karen S. Renzaglia.

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Renzaglia, K.S., Lopez, R.A. & Johnson, E.E. Callose is integral to the development of permanent tetrads in the liverwort Sphaerocarpos . Planta 241, 615–627 (2015). https://doi.org/10.1007/s00425-014-2199-7

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