Adaptive evolution in the photosensory domain of phytochrome A in early angiosperms

Molecular Biology and Evolution

Volumn 20, Issue 7, 2003, Pages 1087-1097

  Mathews, Sarah ^a   Burleigh, J Gordon ^a   Donoghue, Michael J ^a  

^a NONE

Author keywords

Adaptive evolution; Early angiosperms; Phytochrome A; Positive selection

Indexed keywords

PHYTOCHROME; PHYTOCHROME A; PHYTOCHROME C; UNCLASSIFIED DRUG;

ADAPTATION; AMINO ACID SUBSTITUTION; ANGIOSPERM; ARTICLE; EVOLUTION; FLOWER; GENE SEQUENCE; GENETIC SELECTION; GENETIC VARIABILITY; HABITAT STRUCTURE; LIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSYNTHESIS; PLANT GENETICS; PROTEIN DOMAIN;

MAGNOLIOPHYTA;

EID: 0038497893     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msg123     Document Type: Article

References (125)

1. Alba, R., P. M. Kelmenson, M. M. Cordonnier-Pratt, and L. H. Pratt. 2000. The phytochrome gene family in tomato and the rapid differential evolution of this family in angiosperms. Mol. Biol. Evol. 17:362-373.
2. Anisimova, M., J. P. Bielawski, and Z. Yang. 2001. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol. Biol. Evol. 18:1585-1592.
3. -. 2002. Accuracy and power of Bayes prediction of amino acid sites under positive selection. Mol. Biol. Evol. 19:950-958.
4. Arber, E. A. N., and J. Parkin. 1907. On the origin of angiosperms. Bot. J. Linn. Soc. 38:29-80.
5. Axelrod, D. I. 1952. A theory of angiosperm evolution. Evolution 6:29-60.
6. Barkman, T. J., G. Chenery, J. R. Mcneal, J. Lyons-Weiler, W. J. Elisens, G. Moore, A. D. Wolfe, and C. W. DePamphilis. 2000. Independent and combined analyses of sequences from all three genomic compartments converge on the root of flowering plant phylogeny. Proc. Natl. Acad. Sci. USA 97:13166-13171.
7. Basu, D., K., Dehesh, H.-J., Schneider-Poetsch, S. E., Harrington, S. R., McCouch, and P. H. Quail, 2000. Rice PHYC gene: structure, expression, map position and evolution. Plant Mol. Biol. 44:27-42.
8. Bergelson, J., M. Kreitman, E. A. Stahl, and D. Tian. 2001. Evolutionary dynamics of plant R-genes. Science 292:2281-2289.
9. Bessey, C. E. 1915. The phylogenetic taxonomy of flowering plants. Ann. Missouri Bot. Gard. 2:109-164.
10. Bews, J. W. 1927. Studies in the ecological evolution of angiosperms. New Phytol. 26:1-21.
11. Bishop, J. G., A. M. Dean, and T. Mitchell-Olds. 2000. Rapid evolution in plant chitinases: molecular targets of selection in plant-pathogen coevolution. Proc. Natl. Acad. Sci. USA 97:5322-5327.
12. Bogorad, L. 1950. Factors associated with the synthesis of chlorophyll in the dark in seedlings of Pinus jeffreyi. Bot. Gaz. 111:221-241.
13. Botto, J. F, R. A. Sanchez, G. C. Whitelam, and J. J. Casal. 1996. Phytochrome A mediates the promotion of seed germination by very low fluences of light and canopy shade light in Arabidopsis. Plant Physiol. 110:439-444.
14. Bower, F. O. 1882. The germination and embryogeny of Gnetum gnemon. Q. J. Micr. Sci. 22:278-298.
15. Burgerstein, A. 1900. Ueber das Verhalten der Gymnospermen-Keimlinge im Licht und im Dunkeln. Ber. Dtsch. Bot. Ges. 18:168-184.
16. Burgin, M. J., J. J. Casal, G. C. Whitelam, and R. A. Sanchez. 1999. A light-regulated pool of phytochrome and rudimentary high-irradiance responses under far-red light in Pinus elliotti and Pseudotsuga menziesii. J. Exp. Bot. 50:831-836.
17. Casal, J. J. 2000. Phytochromes, cryptochromes, phototropin: photoreceptor interactions in plants. Photochem. Photobiol. 71:1-11.
18. Casal, J. J., R. A. Sanchez, and M. J. Yanovsky. 1997. The function of phytochrome A. Plant Cell Environ. 20:813-819.
19. Cerdán, P. D., M. J. Yanovsky, F. C. Reymunds, A. Nagatani, R. J. Staneloni, G. C. Whitelam, and J. J. Casal. 1999. Regulation of phytochrome B signaling by phytochrome A and FHY1 in Arabidopsis thaliana. Plant J. 18:499-507.
20. Chen, R. A., A. Greer, and A. M. Dean. 1995. A highly active decarboxylating dehydrogenase with rationally inverted coenzyme specificity. Proc. Natl. Acad. Sci. USA 92:11666-11670.
21. -. 1996. Redesigning secondary structure to invert coenzyme specificity in isopropylmalate dehydrogenase. Proc. Natl. Acad. Sci. USA 93:12171-12176.
22. Chinn, E., and J. Silverthorne. 1993. Light-dependent chloroplast development and expression of a light-harvesting chlorophyll a/b-binding protein gene in the gymnosperm Ginkgo biloba. Plant Physiol. 103:727-732.
23. Christensen, S., E. Laverne, G. Boyd, and J. Silverthorne. 2002. Ginkgo biloba retains functions of both type I and type II flowering plant phytochrome. Plant Cell Physiol. 43:768-777.
24. Clapham, D. H., H. Ü. Kolukisaoglu, C.-T. Larsson, M. Qamaruddin, I. Ekberg, C. Wiegmann-Eirund, H. A. W. Schneider-Poetsch, and S. Von Arnold. 1999. Phytochrome types in Picea and Pinus. Expression patterns of PHYA-related types. Plant Mol. Biol. 40:669-678.
25. Crandall, K. A., C. R. Kelsey, H. Imamichi, H. C. Lane, and N. P. Salzman. 1999. Parallel evolution of drug resistance in HIV: failure of nonsynonymous/synonymous substitution rate ratio to detect selection. Mol. Biol. Evol. 16:372-382.
26. Crane, P. R., E. M., Friis, and K. R. Pederson, 1995. The origin and early diversification of angiosperms. Nature 374:27-33.
27. Cronquist, A. 1988. The evolution and classification of flowering plants. The New York Botanical Garden, New York.
28. Cunningham, C. W., K. E. Omland, and T. H. Oakley. 1998. Reconstructing ancestral character states: a critical reappraisal. Trends Ecol. Evol. 13:361-366.
29. Doyle, J. A. 1978. Origin of angiosperms. Annu. Rev. Ecol. Syst. 9:365-392.
30. Doyle, J. A., and M. J. Donoghue. 1986. Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Bot. Rev. 52:321-431.
31. -. 1993. Phylogenies and angiosperm diversification. Paleobiology 19:141-167.
32. Doyle, J. A., and P. K. Endress. 2000. Morphological phylogenetic analysis of basal angiosperms: comparison and combination with molecular data. Int. J. Plant Sci. 161:S121-S153.
33. Doyle, J. A., and L. J. Hickey. 1976. Pollen and leaves from the mid-Cretaceous Potomac group and their bearing on early angiosperm evolution. Pp. 139-206 in C. B. Beck, ed. Origin and early evolution of angiosperms. Columbia University Press, New York.
34. Dykhuizen, D., and D. L. Hartl. 1980. Selective neutrality of 6PGD allozymes in E. coli and the effects of genetic background. Genetics 96:801-817.
35. Eichenberg, K., I. Baurle, N. Paulo, R. A. Sharrock, W. Rudiger, and E. Schafer. 2000. Arabidopsis phytochromes C and E have different spectral characteristics from those of phytochromes A and B. FEBS Lett. 470:107-112.
36. Endo, T., K. Ikeo, and T. Gojobori. 1996. Large-scale search for genes on which positive selection may operate. Mol. Biol. Evol. 13:685-690.
37. Fankhauser, C., and J. Chory. 1997. Light control of development. Annu. Rev. Cell Dev. Biol. 13:203-229.
38. Feild, T. S., N. C. Arens, and T. E. Dawson. 2003. Emerging perspectives on the ancestral ecophysiology of angiosperms. Intl. J. Plant Sci. In press.
39. Force, A., M. Lynch, F. B. Pickett, A. Amores, Y. Yan, and J. Postlethwait. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545.
40. Friis, E. M., W. G., Chalconer, and Crane, P. R. 1987. The origins of angiosperms and their biological consequences. Cambridge University Press, Cambridge.
41. Furuya, M. and E. Schäfer. 1996. Photoperception and signaling of induction reactions by different phytochromes. Trends Plant Sci. 1:301-306.
42. Golding, G. B., and A. M. Dean. 1998. The structural basis of molecular adaptation. Mol. Biol. Evol. 15:355-369.
43. Goldman, N., and Z. Yang. 1994. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol. Biol. Evol. 11:725-736.
44. Graham, S. W., P. A. Reeves, A. C. E. Bums, and R. G. Olmstead. 2000. Microstructural characters in noncoding chloroplast DNA: interpretation, evolution, and utility of indels and inversions in basal angiosperm phylogenetic inference. Int. J. Plant Sci. 161(Suppl.):S83-S96.
45. Grubb, P. J. 1998. Seeds and fruits of tropical rainforest plants: interpretation of the range of seed size, degree of defense, and flesh/seed quotients. Pp. 1-24 in D. M. Newberry, H. H. T. Prins, and N. D. Brown, eds. Dynamics of tropical communities. Blackwell Scientific, Oxford.
46. Gu, X. 1999. Statistical method for testing functional divergence after gene duplication. Mol. Biol. Evol. 16:1664-1674.
47. -. 2001. Maximum-likelihood approach for gene family evolution under functional divergence. Mol. Biol. Evol. 18:453-464.
48. Hall, B. G. 1984. The evolved β-galactosidase system of Escherichia coli. Pp. 165-185 in R. P. Mortlock, ed. Microorganisms as model systems for studying evolution. Plenum Press, New York.
49. Halliday, K. J., B. Thomas, and G. C. Whitelam. 1997. Expression of heterologous phytochromes A, B, or C in transgenic tobacco plants alters vegetative development and flowering time. Plant J. 12:1079-1090.
50. Hennig, L., W. M. Stoddart, M. Dieterle, G. C. Whitelam, and E. Schäfer. 2002. Phytochrome E controls light-induced germination in Arabidopsis. Plant Physiol. 128:194-200.
51. Hickey, L. J., and J. A. Doyle. 1977. Early Cretaceous fossil evidence for angiosperm evolution. Bot. Rev. 43:1-104.
52. Hill, R. E., and N. D. Hastie. 1987. Accelerated evolution in the reactive centre regions of serine protease inhibitors. Nature 326:96-99.
53. Huelsenbeck, J. P., and F. R. Ronquist. 2001. MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754-755.
54. Hughes, A. L. 1999. Adaptive evolution of genes and genomes. Oxford University Press, New York.
55. Kendrick, R. E., and G. H. M. Kronenberg. 1994. Photomorphogenesis in plants. Kluwer Academic, Dordrecht, The Netherlands.
56. Knoll, A. H. 1984. Patterns of extinction in the fossil record of vascular plants. Pp. 21-68 in M. H. Nitecki, ed. Extinctions. University of Chicago Press, Chicago.
57. Lidgard, S., and P. R. Crane. 1988. Quantitative analyses of the early angiosperm radiation. Nature 331:344-346.
58. Lupia, R., S. Lidgard, and P. R. Crane. 1999. Comparing palynological abundance and diversity: implications for biotic replacement during the Cretaceous angiosperm radiation. Paleobiology 25:305-340.
59. Lynch, M., and J. S. Conery. 2000. The evolutionary fate and consequences of duplicate genes. Science 290:1151-1155.
60. Lynch, M., and A. Force. 2000. The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459-473.
61. Maddison, D. R., and W. P. Maddison. 2000. MacClade 4. Analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, Mass.
62. Maloof, J., J. O. Borevitz, T. Dabi et al. (11 co-authors). 2001. Natural variation in light sensitivity of Arabidopsis. Nat. Genet. 29:441-446.
63. Mathews, S., and M. J. Donoghue. 1999. The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 286:947-950.
64. -. 2000. Basal angiosperm phylogeny inferred from duplicate phytochromes A and C. Int. J. Plant Sci. 161(Suppl. 6):S41-S55.
65. Mathews, S., M. Lavin, and R. A. Sharrock. 1995. Evolution of the phytochrome gene family and its utility for phylogenetic analyses of angiosperms. Ann. Missouri Bot. Gard. 82:296-321.
66. Mathews, S., and R. A. Sharrock. 1997. Phytochrome gene diversity. Plant Cell Environ. 20:666-671.
67. McCormac, A. C., G. C. Whitelam, M. T. Boylan, P. H. Quail, and H. Smith. 1992. Contrasting responses of etiolated and light-adapted seedlings to red:far-red ratio: a comparison of wild type, mutant and transgenic plants has revealed differential functions of members of the phytochrome family. J. Plant Physiol. 140:707-714.
68. McNellis, T. W., and X.-W. Deng. 1995. Light control of seedling morphogenetic pattern. Plant Cell 7:1749-1761.
69. Metcalfe, D. J., and P. J. Grubb. 1997. The responses to shade of seedlings of very small-seeded tree and shrub species from tropical rain forest in Singapore. Funct. Ecol. 11:215-221.
70. Montgomery, B. L., and J. C. Lagarias. 2002. Phytochrome ancestry: sensors of bilins and light. Trends Plant Sci. 7:357-366.
71. Mukai, Y., K. Tazaki, T. Fujii, and N. Yamamoto. 1992. Light-independent expression of three photosynthetic genes, cab, rbcS, and rbcL, in coniferous plants. Plant Cell Physiol. 33:859-866.
72. Nagatani, A., J. W. Reed, and J. Chory. 1993. Isolation and initial characterization of Arabidopsis mutants that are deficient in phytochrome A. Plant Physiol. 102:269-277.
73. Newcomb, R. D., P. M. Campbell, D. L. Ollis, E. Cheah, R. J. Russell, and J. G. Oakshott. 1997. A single amino acid substitution converts a carboxylesterase to an organophosphorous hydrolase and confers insecticide resistance on a blowfly. Proc. Natl. Acad. Sci. USA 94:7464-7468.
74. Nielsen, R., and Z. Yang. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929-936.
75. Ohno, S. 1970. Evolution by gene duplication. Springer-Verlag, Berlin.
76. Parkinson, C. L., K. L. Adams, and J. D. Palmer. 1999. Multigene analyses identify the three earliest lineages of extant flowering plants. Curr. Biol. 9:1485-1488.
77. Parks, B. M., and P. H. Quail. 1993. hy8, a new class of Arabiodopsis long hypocotyl mutants deficient in functional phytochrome A. Plant Cell 5:39-48.
78. Perutz, M. F. 1983. Species adaptation in a protein molecule. Mol. Biol. Evol. 1:1-28.
79. Pigliucci, M., and J. Schmitt. 1999. Genes affecting phenotypic plasticity in Arabidopsis: pleiotropic effects and reproductive fitness of photomorphogenic mutants. J. Evol. Biol. 12:551-562.
80. Qin, M., R. Kuhn, S. Moran, and P. H. Quail. 1997. Overexpressed phytochrome C has similar photosensory specificity to phytochrome B but a distinctive capacity to enhance primary leaf expansion. Plant J. 12:1163-1172.
81. Qiu, Y.-L., J. Lee, F. Bernasconi-Quadroni, D. E. Soltis, P. S. Soltis, M. Zanis, E. A. Zimmer, Z. Chen, V. Savolainen, and M. W. Chase. 1999. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402:404-407.
82. Quail, P. H. 1991. Phytochrome: a light-activated molecular switch that regulates plant gene expression. Annu. Rev. Genet. 25:389-409.
83. Quail, P. H., M. T. Boylan, B. M. Parks, T. W. Short, and D. Wagner. 1995. Phytochromes: photosensory perception and signal transduction. Science 268:675-680.
84. Sanderson, M. J., and J. A. Doyle. 2001. Sources of error and confidence intervals in estimating the age of angiosperms from rbcL and 18S rDNA data. Am. J. Bot. 88:1499-1516.
85. Savolainen, V., M. W. Chase, S. B. Hoot, C. M. Morton, D. E. Soltis, and C. Bayer. 2000. Phylogenetics of flowering plants based on combined analysis of plastid atpB and rbcL gene sequences. Syst. Biol. 49:306-362.
86. Schmidt, M., and H. A. W. Schneider-Poetsch. 2002. The evolution of gymnosperms redrawn by phytochrome genes: The Gnetatae appear at the base of the gymnosperms. J. Mol. Evol. 54:715-724.
87. Schmitt, A., A. C. McCormac, and H. Smith. 1995. A test of the adaptive plasticity hypothesis using transgenic and mutant plants disabled in phytochrome-mediated elongation responses to neighbors. Am. Nat. 146:937-953.
88. Schneider-Poetsch, H. A. W., Ü., Kolukisaoglu, D. H., Clapham, J., Hughes, and Lamparter, T. 1998. Non-angiosperm phytochromes and evolution of vascular plants. Physiol. Plant. 102:612-622.
89. Schluter, D, T. Price, A. Ø. Mooers, and D. Ludwig. 1997. Likelihood of ancestor states in adaptive radiation. Evolution 51:1699-1711.
90. Sharrock, R. A., and P. H. Quail. 1989. Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution and differential expression of a plant regulatory photoreceptor family. Genes Dev. 3:1745-1757.
91. Shinomura, T, K. Uchida, and M. Furuya. 2000. Elementary processes of photoreception by phytochrome A for high-irradiance response of hypocotyl elongation in Arabidopsis. Plant Physiol. 122:147-156.
92. Smith, H. 1995. Physiological and ecological function within the phytochrome family. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46:289-315.
93. -. 2000. Phytochromes and light signal perception by plants - an emerging synthesis. Nature 407:585-591.
94. Smith, H., Y. Xu, and P. H. Quail. 1997. Antagonistic but complementary actions of phytochromes A and B allow optimum seedling de-etiolation. Plant Physiol. 114:637-641.
95. Soltis, P. S., D. E. Soltis, and M. W. Chase. 1999. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402:402-404.
96. Soltis, P. S., D. E. Soltis, M. W. Chase et al. (16 co-authors). 2000. Angiosperm phylogeny inferred from a combined data set of 18s rDNA, rbcL, and atpB sequences. Bot. J. Linn. Soc. 133:381-461.
97. Somers, D. E., R. A. Sharrock, J. M. Tepperman, and P. H. Quail. 1991. The hy3 long hypocotyls mutant of Arabidopsis is deficient in phytochrome B. Plant Cell 3:1263-1274.
98. Stebbins, G. L. 1974. Flowering plants, evolution above the species level. Harvard University Press, Cambridge.
99. Sun, G., Q. Ji, D. L. Dilcher, S. Zheng, K. C. Nixon, and X. Wang. 2002. Archaefructaceae, a new basal angiosperm family. Science 296:899-904.
100. Takano, M., H. Kanegae, T. Shinomura, A. Miyao, H. Hirochika, and M. Furuya. 2001. Isolation and characterization of rice phytochrome A mutants. Plant Cell 13:521-534.
101. Takhtajan, A. L. 1969. Flowering plants: origin and dispersal. Smithsonian Institution, Washington, D.C.
102. Tavaré, S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. Pp. 57-86 in Lectures on mathematics in the life sciences. Vol. 17. American Mathematical Society, Providence, R.I.
103. Taylor, D. W., and L. J. Hickey. 1992. Phylogenetic evidence for the herbaceous origin of angiosperms. Plant Syst. Evol. 180:137-156.
104. -. 1996. Evidence for and implications of an herbaceous origin for angiosperms. Pp. 232-266 in D. Taylor and L. Hickey, eds. Flowering plant origin, evolution, and phylogeny. Chapman and Hall, New York.
105. Thorne, R. F. 1974. A phylogenetic classification of the Annoniflorae. Aliso 8:147-209.
106. Van Tuinen, A., L. H. J. Kerckhoffs, A. Nagatani, R. E. Kendrick, and M. Koornneef. 1995. Far-red light insensitive, phytochrome A deficient mutants of tomato. Mol. Gen. Genet. 246:133-141.
107. Wagner, A. 2001. Birth and death of duplicated genes in completely sequenced eukaryotes. Trends Genet. 17:237-239.
108. Wagner, D., and P. H. Quail. 1995. Mutational analysis of phytochrome B identifies a small COOH-terminal-domain region critical for regulatory activity. Proc. Natl. Acad. Sci. USA 92:8596-8600.
109. Walsh, J. B. 1995. How often do duplicated genes evolve new functions? Genetics 110:345-364.
110. Whitelam, G. C., E. Johnson, J. Peng, P. Carol, M. L. Anderson, J. S. Cowl, and N. P. Harberd. 1993. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 5:757-768.
111. Wilks, H. M, K. W. Hart, R. Feeney, C. R. Dunn, H. Muirhead, W. N. Chia, D. A. Barstow, T. Atkinson, A. R. Clarke, and J. J. Holbrook. 1988. A specific, highly active malate dehydrogenase by redesign of a lactate dehydrogenase framework. Science 242:1541-1544.
112. Wing, S. L., and L. D. Boucher. 1998. Ecological aspects of the Cretaceous flowering plant radiation. Annu. Rev. Earth Planet. Sci. 26:379-421.
113. Wu, S.-H., and J. C. Lagarias. 2000. Defining the bilin lyase domain: lessons from the extended phytochrome superfamily. Biochemistry 39:13487-13495.
114. Yang, Z. 1994. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J. Mol. Evol. 39:306-314.
115. -. 1997. PAML: a program for phylogenetic analysis by maximum likelihood version. CABIOS 13:555-556(http://abacus.gene.ucl.ac.uk/software/paml.html).
116. -. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15:568-573.
117. Yang, Z., and J. P. Bielawski. 2000. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15:496-503.
118. Yang, Z., S. Kumar, and M. Nei. 1995. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141:1641-1650.
119. Yang, Z., and R. Nielsen. 2002. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol. Biol. Evol. 19:908-917.
120. Yang, Z., R. Nielsen, N. Goldman, and A.-M. K. Pedersen. 2000. Codon-substitution models for heterogenous selection pressure at amino acid sites. Genetics 155:431-449.
121. Yang, Z., W. J. Swanson, and V. D. Vacquier. 2000. Maximum-likelihood analysis of molecular adaptation in abalone sperm lysin reveals variable selective pressures among lineages and sites. Mol. Biol. Evol. 17:1446-1455.
122. Yanovsky, M. J., J. J. Casal, and J. P. Luppi. 1997. The VLF loci, polymorphic between ecotypes of Landsberg erecta and Columbia dissect two branches of phytochrome A signaling pathways that correspond to the very-low fluence and high-irradiance responses of phytochrome. Plant J. 12:659-667.
123. Yanovsky, M. J., J. J. Casal, and G. C. Whitelam. 1995. Phytochrome A, phytochrome B and HY4 are involved in hypocotyl growth responses to natural radiation in Arabidopsis: weak de-etiolation of the phyA mutant under dense canopies. Plant Cell Environ. 18:788-794.
124. Yanovsky, M. J., J. P. Luppi, D. Kirchbauer, O. B. Ogorodnikova, V. A. Sineshchekov, E. Adam, S. Kircher, R. J. Staneloni, E. Schäfer, F. Nagy, and J. J. Casal. 2002. Missense mutation in the PAS2 domain of phytochrome A impairs subnuclear localization and a subset of responses. Plant Cell 14:1591-1603.
125. Zanis, M. J., D. E. Soltis, P. S. Soltis, S. Mathews, and M. J. Donoghue. 2002. The root of the angiosperms revisited. Proc. Natl. Acad. Sci. USA 99:6848-6853.