PIN2-like proteins may contribute to the regulation of morphogenetic processes during spermatogenesis in Chara vulgaris

Plant Cell Reports

Volumn 35, Issue 8, 2016, Pages 1655-1669

  Żabka, Aneta ^a   Polit, Justyna Teresa ^a   Winnicki, Konrad ^a   Paciorek, Patrycja ^a   Juszczak, Jolanta ^a   Nowak, Mateusz ^a   Maszewski, Janusz ^a  

^a UNIVERSITY OF LODZ   (Poland)

Author keywords

Callose; Chara vulgaris; IAA; PIN2 like proteins; Polar auxin transport; Spermatogenesis

Indexed keywords

ALGAL PROTEIN; INDOLEACETIC ACID DERIVATIVE;

BIOLOGICAL MODEL; CELL WALL; CHARA; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GAMETOGENESIS; METABOLISM; MORPHOGENESIS;

ALGAL PROTEINS; CELL WALL; CHARA; FLUORESCENT ANTIBODY TECHNIQUE; GAMETOGENESIS; INDOLEACETIC ACIDS; MODELS, BIOLOGICAL; MORPHOGENESIS;

EID: 84962803592     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-016-1979-x     Document Type: Article

References (64)

1. Bannigan A, Wiedemeier AM, Williamson RE, Overall RL, Baskin TI (2006) Cortical microtubule arrays lose uniform alignment between cells and are oryzalin resistant in the Arabidopsis mutant, radially swollen 6. Plant Cell Physiol 47:949–958
2. Basu S, Sun H, Brian L, Quatrano RL, Muday GK (2002) Early embryo development in Fucus distichus is auxin sensitive. Plant Physiol 130:292–302
3. Beilby MJ, Casanova MT (2014) The physiology of Characean cells. Springer, Berlin
4. Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465
5. Bennett TA (2015) PIN proteins and the evolution of plant development. Trends Plant Sci 20:498–507
6. Bennett TA, Liu MM, Aoyama T, Bierfreund NM, Braun M, Coudert Y, Dennis RJ, O’Connor D, Wang XY, White CD, Decker EL, Reski R, Harrison CJ (2014) Plasma membrane-targeted PIN proteins drive shoot development in a moss. Curr Biol 24:2776–2785
7. Boot KJM, Libbenga KR, Hille SC, Offringa R, van Duijn B (2012) Polar auxin transport: an early invention. J Exp Bot 63:4213–4218
8. Braybrook SA, Peaucelle A (2013) Mechano-chemical aspects of organ formation in Arabidopsis thaliana: the relationship between auxin and pectin. PLoS One 8:e57813
9. Chen XY, Kim JY (2009) Callose synthesis in higher plants. Plant Signal Behav 4:489–492
10. Chiappetta A, Fambrini M, Petrarulo M, Rapparini F, Michelotti V, Bruno L, Greco M, Baraldi R, Salvini M, Pugliesi C, Bitonti MB (2009) Ectopic expression of LEAFY COTYLEDON1-LIKE gene and localized auxin accumulation mark embryogenic competence in epiphyllous plants of Helianthus annuus × H. tuberosus. Ann Bot 103:735–747
11. Cooke TJ, Poli DB, Sztein AE, Cohen JD (2002) Evolutionary patterns in auxin action. Plant Mol Biol 49:319–338
12. Demchenko KN, Voitsekhovskaja OV, Pawlowski K (2014) Plasmodesmata without callose and calreticulin in higher plants—open channels for fast symplastic transport? Front Plant Sci 5:74
13. Dhonukshe P, Huang F, Galvan-Ampudia CS, Mähönen AP, Kleine-Vehn J, Xu J, Quint A, Prasad K, Friml J, Scheres B, Offringa R (2010) Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development 137:3245–3255
14. Domozych DS, Sørensen I, Willats WGT (2009) The distribution of cell wall polymers during antheridium development and spermatogenesis in the Charophycean green alga, Chara corallina. Ann Bot 104:1045–1056
15. Feraru E, Friml J (2008) PIN polar targeting. Plant Physiol 147:1553–1559
16. Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, Hooykaas PJ, Palme K, Offringa R (2004) A PINOID-dependent binary switch in apical–basal PIN polar targeting directs auxin efflux. Science 306:862–865
17. Fujita T, Sakaguchi H, Hiwatashi Y, Wagstaff SJ, Ito M, Deguchi H, Sato T, Hasebe M (2008) Convergent evolution of shoots in land plants: lack of auxin polar transport in moss shoots. Evol Dev 10:176–186
18. Godlewski M (1980) Auxin as a factor regulating initiation of mitosis in antheridial filaments of Chara vulgaris L. Biochem Physiol Pflanz 175:314–321
19. Godlewski M (1988) Callose formation in injured cells of the vegetative and generative thallus of Chara vulgaris L. Absence of callose in the process of cytodifferentiation. Acta Soc Bot Pol 57:21–30
20. Han X, Hyun TK, Zhang M, Kumar R, Koh EJ, Kang BH, Lucas WJ, Kim JY (2014) Auxin-callose-mediated plasmodesmal gating is essential for tropic auxin gradient formation and signaling. Dev Cell 28:132–146
21. Hoepflinger MC, Geretschlaeger A, Sommer A, Hoeftberger M, Nishiyama T, Sakayama H, Hammerl P, Tenhaken R, Ueda T, Foissner I (2013) Molecular and biochemical analysis of the first ARA6 homologue, a RAB5 GTPase, from green algae. J Exp Bot 64:5553–5568
22. Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353
23. Křeček P, Skůpa P, Libus J, Naramoto S, Tejos R, Friml J, Zažímalová E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10:249
24. Kwiatkowska M (1988) Symplasmic isolation of Chara vulgaris antheridium and mechanisms regulating the process of spermatogenesis. Protoplasma 142:137–146
25. Kwiatkowska M (1999) Plasmodesmal coupling and cell differentiation in algae. In: van Bel AEJ, van Kesteren WJP (eds) Plasmodesmata. Structure, function, role in cell communication. Springer, Heidelberg, pp 205–224
26. Kwiatkowska M (2003) Plasmodesmal changes are related to different developmental stage of antheridia of Chara species. Protoplasma 222:1–11
27. Kwiatkowska M, Maszewski J (1976) Plasmodesmata between synchronously and asynchronously developing cells of the antheridial filaments of Chara vulgaris L. Protoplasma 87:317–327
28. Kwiatkowska M, Maszewski J (1985) Changes in ultrastructure of plasmodesmata during spermatogenesis in Chara vulgaris L. Planta 166:46–50
29. Kwiatkowska M, Maszewski J (1986) Changes in the occurrence and ultrastructure of plasmodesmata in antheridia of Chara vulgaris L. during different stages of spermatogenesis. Protoplasma 132:179–188
30. Kwiatkowska M, Maszewski J (1987a) Ultrastructural and autoradiographic studies of non-generative cells in the antheridium of Chara vulgaris. II. Capitular cells. Folia Histochem Cytobiol 25:225–231
31. Kwiatkowska M, Maszewski J (1987b) Ultrastructural and autoradiographic studies of non-generative cells in the antheridium of Chara vulgaris. I. Manubria. Folia Histochem Cytobiol 25:215–223
32. Kwiatkowska M, Popłońska K, Żylińska K (1990) Biological role of endoreplication in the process of spermatogenesis in Chara vulgaris L. Protoplasma 155:176–187
33. Laskowski M, Grieneisen VA, Hofhuis H, Hove CA, Hogeweg P, Marée AF, Scheres B (2008) Root system architecture from coupling cell shape to auxin transport. PLoS Biol 6:e307
34. Lau S, Jürgens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant Cell 20:1738–1746
35. Lau S, Shao N, Bock R, Jürgens G, De Smet I (2009) Auxin signaling in algal lineages: fact or myth? Trends Plant Sci 14:182–188
36. Le Bail A, Billoud B, Kowalczyk N, Kowalczyk M, Gicquel M, Le Panse S, Stewart S, Scornet D, Cock JM, Ljung K, Charrier B (2010) Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant Physiol 153:128–144
37. Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, Delwiche CF, De Clerck O (2012) Phylogeny and molecular evolution of the green algae. Crit Rev Plant Sci 31:1–46
38. Levy A, Erlanger M, Rosenthal M, Epel BL (2007) A plasmodesmata associated β-1,3-glucanase in Arabidopsis. Plant J 49:669–682
39. Lewis DR, Olex AL, Lundy SR, Turkett WH, Fetrow JS, Muday GK (2013) A kinetic analysis of the auxin transcriptome reveals cell wall remodeling proteins that modulate lateral root development in Arabidopsis. Plant Cell 25:3329–3346
40. Lucas WJ, Ding B, Van der Schoot C (1993) Plasmodesmata and the supracellular nature of plants. New Phytol 125:435–476
41. Maszewski J (1991) Endopolyploidization patterns in non-generative antheridial cells in mono- and dioecious Chara spp. (Characeae) with different DNA C-values. Plant Syst Evol 177:39–52
42. Maszewski J, Kołodziejczyk P (1991) Cell cycle duration in antheridial filaments of Chara spp. (Characeae) with different genome size and heterochromatin content. Plant Syst Evol 175:23–38
43. Maszewski J, van Bel AJE (1996) Different patterns of intercellular transport of Lucifer Yellow in young and mature antheridia of Chara vulgaris L. Bot Acta 109:110–114
44. Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler MG, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz EM, Luschnig C, Offringa R, Friml J (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130:1044–1056
45. Müller A, Guan C, Gälweiler L, Taenzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17:6903–6911
46. Nafisi M, Fimognari L, Sakuragi Y (2015) Interplays between the cell wall and phytohormones in interaction between plants and necrotrophic pathogens. Phytochemistry 112:63–71
47. Olszewska MJ, Godlewski M (1973) A cytochemical study of spermatogenesis in Chara vulgaris L. Folia Histochem Cytobiol 11:9–20
48. Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harb Perspect Biol 2:001537
49. Piazza P, Jasinski S, Tsiantis M (2005) Evolution of leaf developmental mechanisms. New Phytol 167:693–710
50. Pickett-Heaps JD (1967) Ultrastructure and differentiation in Chara sp. I. Vegetative cells. Aust J Biol Sci 20:539–551
51. Pickett-Heaps JD (1968) Ultrastructure and differentiation in Chara sp. III. Formation of the antheridium. Aust J Biol Sci 21:255–274
52. Polevoi VV, Tarakhovskaya ER, Maslov YI, Polevoi AV (2003) Role of auxin in induction of polarity in Fucus vesiculosus zygotes. Russ J Dev Biol 34:360–364
53. Qiu Y-L (2008) Phylogeny and evolution of charophytic algae and land plants. J Syst Evol 46:287–306
54. Quader H, Hofmann A, Schnepf E (1989) Reorganization of the endoplasmic reticulum in epidermal cells of onion bulb scales after cold stress: involvement of cytoskeletal elements. Planta 177:273–280
55. Rahman A, Takahashi M, Shibasaki K, Wu S, Inaba T, Tsurumi S, Baskin TI (2010) Gravitropism of Arabidopsis thaliana roots requires the polarization of PIN2 toward the root tip in meristematic cortical cells. Plant Cell 22:1762–1776
56. Swarup R, Péret B (2012) AUX/LAX family of auxin influx carriers—an overview. Front Plant Sci 3:225
57. Teleżyński H (1929) Garnitures des chromosomes et synchronisme des divisions dans les filaments d’antherozoides chez certaines especes du genre Chara Vaill. Acta Soc Bot Pol 6:230–247
58. Terasaki M (1989) Fluorescent labeling of endoplasmic reticulum. Methods Cell Biol 29:125–135
59. Turmel M, Otis C, Lemieux C (2003) The mitochondrial genome of Chara vulgaris: insights into the mitochondrial DNA architecture of the last common ancestor of green algae and land plants. Plant Cell 15:1888–1903
60. Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016
61. Viaene T, Landberg K, Thelander M, Medvecka E, Pederson E, Feraru E, Cooper ED, Karimi M, Delwiche CF, Ljung K, Geisler M, Sundberg E, Friml J (2014) Directional auxin transport mechanisms in early diverging land plants. Curr Biol 24:2786–2791
62. Żabka A, Trzaskoma P, Winnicki K, Polit JT, Chmielnicka A, Maszewski J (2015) The biphasic interphase-mitotic polarity of cell nuclei induced under DNA replication stress seems to be correlated with Pin2 localization in root meristems of Allium cepa. J Plant Physiol 174:62–70
63. Zažímalová E, Murphy AS, Yang H, Hoyerová K, Hošek P (2010) Auxin transporters—why so many? Cold Spring Harb Perspect Biol 2:a001552
64. Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64