Cell-specific transcriptomic analyses of three-dimensional shoot development in the moss Physcomitrella patens

Plant Journal

Volumn 83, Issue 4, 2015, Pages 743-751

  Frank, Margaret H ^a,b   Scanlon, Michael J ^a  

^a Department of Obstetrics Gynecology   (United States)

^b DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

Author keywords

asymmetric cell division; laser microdissection RNAseq; Physcomitrella patens; shoot apex; stem cell; three dimensional growth

Indexed keywords

CELL PROLIFERATION; GENES; PLANTS (BOTANY); STEM CELLS;

ASYMMETRIC-CELLS; LASER MICRO DISSECTIONS; PHYSCOMITRELLA PATENS; SHOOT APEX; THREE-DIMENSIONAL GROWTH;

CYTOLOGY;

ALGAE; BRYOPHYTA; CHAROPHYCEAE; PHYSCOMITRELLA PATENS;

BRYOPSIDA; CYTOLOGY; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING;

BRYOPSIDA; GENE EXPRESSION REGULATION, PLANT;

EID: 84938949945     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12928     Document Type: Article

References (84)

1. Abe, M., Katsumata, H., Komeda, Y., and, Takahashi, T., (2003) Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development, 130, 635-643.
2. Aoyama, T., Hiwatashi, Y., Shigyo, M., Kofuji, R., Kubo, M., Ito, M., and, Hasebe, M., (2012) AP2-type transcription factors determine stem cell identity in the moss Physcomitrella patens. Development, 139, 3120-3129.
3. Arif, M.A., Fattash, I., Ma, Z., Cho, S.H., Beike, A.K., Reski, R., Axtell, M.J., and, Frank, W., (2012) DICER-LIKE3 activity in Physcomitrella patens DICER-LIKE4 mutants causes severe developmental dysfunction and sterility. Mol. Plant, 5, 1281-1294.
4. Ashton, N.W., Grimsley, N.H., and, Cove, D.J., (1979) Analysis of gametophytic development in the moss Physcomitrella patens, using auxin and cytokinin resistant mutants. Planta, 144, 427-435.
5. Axtell, M.J., (2009) The small RNAs of Physcomitrella patens: expression, function and evolution. Annu. Plant Rev. 36, 113-142.
6. Axtell, M.J., and, Bartel, D.P., (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell, 24, 4837-4849.
7. Axtell, M.J., and, Bowman, J.L., (2008) Evolution of plant microRNAs and their targets. Trends Plant Sci. 13, 343-349.
8. Axtell, M.J., Snyder, J.A., and, Bartel, D.P., (2007) Common functions for diverse small RNAs of land plants. Plant Cell, 19, 1750-1769.
9. Becraft, P.W., Kang, S.-H., and, Suh, S.-G., (2001) The maize CRINKLY4 receptor kinase controls a cell-autonomous differentiation response. Plant Physiol. 127, 486-496.
10. Becraft, P.W., Li, K.J., Dey, N., and, Asuncion-Crabb, Y., (2002) The maize dek1 gene functions in embryonic pattern formation and cell fate specification. Development, 129, 5217-5225.
11. Benjamins, R., Quint, A., Weijers, D., Hooykaas, P., and, Offringa, R., (2001) The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development, 128, 4057-4067.
12. Bennett, T.A., Liu, M.M., Aoyama, T., et al., (2014) Plasma membrane-targeted PIN proteins drive shoot development in a moss. Curr. Biol. 24, 2776-2785.
13. Bullard, J.H., Purdom, E., Hansen, K.D., and, Dudoit, S., (2010) Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics, 11, 94.
14. Busch, H., Boerries, M., Bao, J., Hanke, S.T., Hiss, M., Tiko, T., and, Rensing, S.A., (2013) Network theory inspired analysis of time-resolved expression data reveals key players guiding P. patens stem cell development. PLoS One, 8, e60494.
15. Chevalier, D., Batoux, M., Fulton, L., Pfister, K., Yadav, R.K., Schellenberg, M., and, Schneitz, K., (2005) STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. Proc. Natl Acad. Sci. USA, 102, 9074-9079.
16. Cho, S.H., Coruh, C., and, Axtell, M.J., (2012) miR156 and miR390 regulate tasiRNA accumulation and developmental timing in Physcomitrella patens. Plant Cell, 24, 4837-4849.
17. Chou, H.H., and, Holmes, M.H., (2001) DNA sequence quality trimming and vector removal. Bioinformatics, 17, 1093-1104.
18. Cole, M., Jacobs, B., Soubigou-Taconnat, L., Balzergue, S., Renou, J.P., Chandler, J.W., and, Werr, W., (2013) Live imaging of DORNRÖSCHEN and DORNRÖSCHEN-LIKE promoter activity reveals dynamic changes in cell identity at the microcallus surface of Arabidopsis embryonic suspensions. Plant Cell Rep. 32, 45-59.
19. Cove, D.J., and, Knight, C.D., (1993) The moss Physcomitrella patens, a model system with potential for the study of plant reproduction. Plant Cell, 5, 1483-1488.
20. Cove, D.J., Perroud, P.-F., Charron, A.J., McDaniel, S.F., Khandelwal, A., and, Quatrano, R.S., (2009) The moss Physcomitrella patens: a novel system for plant development and genomic studies. Cold Spring Harb. Protoc. pdb.emo115. doi: 10.1101/pdb.emo115.
21. Demko, V., Perroud, P.-F., Johansen, W., et al., (2014) Genetic analysis of DEFECTIVE KERNEL1 loop function in three-dimensional body patterning in Physcomitrella patens. Plant Physiol. 166, 903-919.
22. Dewitte, W., Sofield, S., Alcasabas, A.A., et al. (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc. Natl Acad. Sci. USA, 104, 14537-14542.
23. DeYoung, B.J., Bickle, K.L., and, Schrage, K.J., (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J. 45, 1-16.
24. Dong, J., and, Bergmann, D.C., (2010) Stomatal patterning and development. Curr. Top. Dev. Biol. 91, 267-297.
25. Eyüboglu, B., Pfister, K., Haberer, G., Chevalier, D., Fuchs, A., Mayer, K.F.X., and, Schneitz, K., (2007) Molecular characterisation of the STRUBBELIG-RECEPTOR FAMILY of genes encoding putative leucine-rich repeat receptor-like kinases in Arabidopsis thaliana. BMC Plant Biol. 7, 16.
26. Frank, M.H., and, Scanlon, M.J., (2015) Transcriptomic evidence for the evolution of shoot meristem function in sporophyte-dominant land plants through concerted selection of ancestral gametophytic and sporophytic genetic programs. Mol. Biol. Evol. 32, 355-367.
27. Graham, L.K., and, Wilcox, L.W., (2000) The origin of alternation of generations in land plants: a focus on matrotrophy and hexose transport. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 757-767.
28. Guyomarc'h, S., Bertrand, C., Delarue, M., and, Zhou, D.X., (2005) Regulation of meristem activity by chromatin remodeling. Trends Plant Sci. 10, 332-338.
29. Harrison, C.J., Roeder, A.H.K., Meyerowitz, E.M., and, Langdale, J.A., (2009) Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens. Curr. Biol. 19, 461-471.
30. Hay, A., and, Tsiantis, M., (2010) KNOX genes: versatile regulators of plant development and diversity. Development, 137, 3153-3165.
31. Heidstra, R., (2007) Asymmetric cell division in plant development. Prog. Mol. Subcell. Biol. 45, 1-37.
32. Hord, C.L.H., Chen, C., DeYoung, B.J., Clark, S.E., and, Ma, H., (2006) The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell, 18, 1667-1680.
33. Inagaki, S., and, Umeda, M., (2011) Cell-cycle control and plant development. Int. Rev. Cell Mol. Biol. 291, 227-261.
34. Ishikawa, M., and, Hasebe, M., (2015) Cell cycle reentry from the late S phase: implications from stem cell formation in the moss Physcomitrella patens. J. Plant. Res. 128, 399-405.
35. Ishikawa, M., Murata, T., Sato, Y., et al. (2011) Physcomitrella cyclin-dependent kinase A links cell cycle reactivation to other cellular changes during reprogramming of leaf cells. Plant Cell, 23, 2924-2938.
36. Jang, G., and, Dolan, L., (2011) Auxin promotes the transition from chloronema to caulonema in moss protonema by positively regulating PpRSL1 and PpRSL2 in Physcomitrella patens. New Phytol. 192, 319-327.
37. Johri, M.M., and, Desai, S., (1973) Auxin regulation of caulonema formation in moss protonema. Nat. New Biol. 245, 223-224.
38. Kanaoka, M.M., Pillitteri, L.J., Fujii, H., and, Yoshida, Y., (2008) SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell, 20, 1775-1785.
39. Karol, K.G., McCourt, R.M., Cimino, M.T., and, Delwiche, C.F., (2001) The closest living relatives of land plants. Science, 294, 2351-2353.
40. Khraiwesh, B., Arif, M.A., Seumel, G.I., and, Ossowski, S., (2010) Transcriptional control of gene expression by microRNAs. Cell, 140, 111-122.
41. Kofuji, R., and, Hasebe, M., (2014) Eight types of stem cells in the life cycle of the moss Physcomitrella patens. Curr. Opin. Plant Biol. 17, 13-21.
42. Kumar, R., Ichihashi, Y., Kimura, S., Chitwood, D.H., Headland, L.R., Peng, J., Maloof, J.N., and, Sinha, N.R., (2012) A high-throughput method for Illumina RNA-Seq library preparation. Front. Plant Sci. 3, 302.
43. Kwon, C.S., Chen, C.B., and, Wagner, D., (2005) WUSCHEL is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem cell fate in Arabidopsis. Genes Dev. 19, 992-1003.
44. Larionov, A., Krause, A., and, Miller, W., (2005) A standard curve based method for relative real time PCR data processing. BMC Bioinformatics, 6, 62.
45. Li, S., and, Chou, H.H., (2004) LUCY2: an interactive DNA sequence quality trimming and vector removal tool. Bioinformatics, 20, 2865-2866.
46. Lid, S.E., Gruis, D., Jung, R., Lorentzen, J.A., Ananiey, E., Chamberlin, M., Niu, X., Meely, R., Nichols, S., and, Olsen, O.A., (2002) The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily. Proc. Natl Acad. Sci. USA, 99, 5460-5465.
47. Lukowitz, W., Roeder, A., Parmenter, D., and, Somerville, C., (2004) A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell, 116, 109-119.
48. Mandel, T., Moreau, F., Kutsher, Y., and, Fletcher, J.C., (2014) The ERECTA receptor kinase regulates Arabidopsis shoot apical meristem size, phyllotaxy and floral meristem identity. Development, 141, 830-841.
49. McCourt, R.M., Delwiche, C.F., and, Karol, K.G., (2004) Charophyte algae and land plant origins. Trends Ecol. Evol. 19, 661-666.
50. Menand, B., Yi, K., Jouannic, S., Hoffman, L., Ryan, E., Linstead, P., Schaefer, D.G., and, Dolan, L., (2007) An ancient mechanism control the development of cells with a rooting function in land plants. Science, 316, 1477-1480.
51. Menges, M., de Jager, S.M., Gruissem, W., and, Murray, J.A.H., (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J. 41, 546-566.
52. Mosquna, A., Katz, A., Decker, E.L., Rensing, S.A., Reski, R., and, Ohad, N., (2009) Regulation of stem cell maintenance by the Polycomb protein FIE has been conserved during land plant evolution. Development, 136, 2433-2444.
53. Nettleton, D., Hwang, J.T.G., Caldo, R.A., and, Wise, R.P., (2006) Estimating the number of true null hypotheses from a histogram of p values. J. Agric. Biol. Environ. Stat. 11, 337-356.
54. Niklas, K.J., (1997) The Evolutionary Biology of Plants. Chicago: The University of Chicago Press.
55. Niklas, K.J., (2000) The evolution of plant body plans-a biomechanical perspective. Ann. Bot. 36, 411-438.
56. Niklas, K.J., and, Kutschera, U., (2009) The evolutionary development of plant body plans. Funct. Plant Biol. 36, 682.
57. Niklas, K.J., and, Kutschera, U., (2010) The evolution of the land plant life cycle. New Phytol. 185, 27-41.
58. Nishiyama, T., Hiwatashi, Y., Sakakibara, K., Kato, M., and, Hasebe, M., (2000) Tagged mutagenesis and gene-trap in the moss, Physcomitrella patens by shuttle mutagenesis. DNA Res. 7, 9-17.
59. Nishiyama, T., Miyawaki, K., Ohshima, M., Thompson, K., Nagashima, A., Hasebe, M., and, Kurata, T., (2012) Digital gene expression profiling by 5′-end sequencing of cDNAs during reprogramming in the moss Physcomitrella patens. PLoS ONE, 7, e36461.
60. Okano, Y., Aono, N., Hiwatashi, Y., Murata, T., Nishiyama, T., Ishikawa, T., Kubo, M., Hasebe, M., and, Crane, P.R., (2009) A polycomb repressive complex 2 gene regulates apogamy and gives evolutionary insights into early land plant evolution. Proc. Natl Acad. Sci. USA, 106, 16321-16326.
61. Perroud, P.E., Demko, V., Johansen, W., Wilson, B.C., Olsen, O.A., and, Quatrano, R.S., (2014) Defective Kernel 1 (DEK1) is required for three-dimensional growth in Physcomitrella patens. New Phytol. 203, 794-804.
62. Pires, N.D., Yi, K., Breuninger, H., Catarino, B., Menand, B., and, Dolan, L., (2013) Recruitment and remodeling of an ancient gene regulatory network during land plant evolution. Proc. Natl Acad. Sci. USA, 110, 9571-9576.
63. Rensing, S.A., Lang, D., Zimmer, A.D., et al. (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science, 319, 64-69.
64. Rounds, C.M., and, Bezanilla, M., (2013) Growth mechanisms in tip-growing plant cells. Annu. Rev. Plant Biol. 64, 243-265.
65. Ruszala, E.M., Beerling, D.J., Franks, P.J., and, Chater, C., (2011) Land plants acquired active stomatal control early in their evolutionary history. Curr. Biol. 21, 1030-1035.
66. Sakakibara, K., Nishiyama, T., Deguchi, H., and, Hasebe, M., (2008) Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development. Evol. Dev. 10, 555-566.
67. Sakakibara, K., Ando, S., Yip, H.K., Tamada, Y., and, Hiwatashi, Y., (2013) KNOX2 genes regulate the haploid-to-diploid morphological transition in land plants. Science, 339, 1067-1070.
68. Sakakibara, K., Reisewitz, P., Aoyama, T., et al. (2014) WOX13-like genes are required for reprogramming of leaf and protoplast cells into stem cells in the moss Physcomitrella patens. Development, 141, 1660-1670.
69. Saleh, O., Issman, N., Seumel, G.I., Stav, R., Samach, A., Reski, R., Frank, W., and, Arazi, T., (2011) MicroRNA534a control of BLADE-ON-PETIOLE 1 and 2 mediates juvenile-to-adult gametophyte transition in Physcomitrella patens. Plant J. 65, 661-674.
70. Scanlon, M.J., Ohtsu, K., and, Timmermans, M., (2009) Laser microdissection-mediated isolation and in vitro transcriptional amplification of plant RNA. Curr. Protoc. Mol. Biol. 87A, 25A.3.1-25A.3.15.
71. Singer, S.D., and, Ashton, N.W., (2007) Revelation of ancestral roles of KNOX genes by a functional analysis of Physcomitrella homologues. Plant Cell Rep. 26, 2039-2054.
72. Steeves, T.A., and, Sussex, I.M., (1989) Patterns in Plant Development. Cambridge: Cambridge University Press.
73. Talmor-Neiman, M., Stav, R., Frank, W., Voss, B., and, Arazi, T., (2006) Novel micro-RNAs and intermediates of micro-RNA biogenesis from moss. Plant J. 47, 25-37.
74. Thelander, M., Olsson, T., and, Ronne, H., (2005) Effect of the energy supply on filamentous growth and development in Physcomitrella patens. J. Exp. Bot. 56, 653-662.
75. Vatén, A., and, Bergmann, D.C., (2012) Mechanisms of stomatal development: an evolutionary view. EvoDevo, 3, 11.
76. Vidali, L., and, Bezanilla, M., (2012) Physcomitrella patens: a model for tip cell growth and differentiation. Curr. Opin. Plant Biol. 15, 625-631.
77. Vollbrecht, E., Veiti, B., Sinha, N.R., and, Hake, S., (1991) The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature, 350, 241-243.
78. Weigel, D., Alvarez, J., Smyth, D.R., and, Yanofsky, M.F., (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell, 69, 843-859.
79. Widiez, T., Symeonidi, A., Luo, C., Lam, E., Lawton, M., and, Rensing, S.A., (2014) The chromatin landscape of the moss Physcomitrella patens and its dynamics during development and drought stress. Plant J. 79, 67-81.
80. Wildwater, M., Campilho, A., Perez-Perez, J.M., Heidstra, R., Blilou, I., Korthout, H., Chatterjee, J., Mariconti, L., Gruissem, W., and, Scheres, B., (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell, 123, 1337-1349.
81. Wu, T.D., and, Nacu, S., (2010) Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics, 26, 873-881.
82. Xiao, L., Wang, H., Wan, P., Kuang, T., and, He, Y., (2011) Genome-wide transcriptome analysis of gametophyte development in Physcomitrella patens. BMC Plant Biol. 11, 177.
83. Xiao, L., Zhang, L., Yang, G., Zhu, H., and, He, Y., (2012) Transcriptome of protoplasts reprogrammed into stem cells in Physcomitrella patens. PLoS One, 7, e35961.
84. Zimmer, A.D., Lang, D., Buchta, K., Rombauts, S., Nishiyama, T., Hasebe, M., Van de Peer, Y., Rensing, S.A., and, Reski, R., (2013) Reannotation and extended community resources for the genome of the non-seed plant Physcomitrella patens provide insights into the evolution of plant gene structures and functions. BMC Genom. 14, 498.