Plant genetics: a decade of integration

Article metrics

Abstract

The last decade provided the plant science community with the complete genome sequence of Arabidopsis thaliana and rice, tools to investigate the function of potentially every plant gene, methods to dissect virtually any aspect of the plant life cycle, and a wealth of information on gene expression and protein function. Focusing on Arabidopsis as a model system has led to an integration of the plant sciences that triggered the development of new technologies and concepts benefiting plant research in general. These enormous changes led to an unprecedented increase in our understanding of the genetic basis and molecular mechanisms of developmental, physiological and biochemical processes, some of which will be discussed in this article.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Progress in our molecular genetic understanding of flower development.
Figure 2: Plants respond to environmental light conditions through several distinct photoreceptors with sensitivities ranging from far-red/red in phytochromes, to blue/ultraviolet-A in cryptochromes and phototropins, to ultraviolet-B in as yet unidentified receptors (top)62,63,64,65,66,67.
Figure 3: Plant-pathogen interactions.
Figure 4: From QTL to QTN.
Figure 5: Epigenetic phenomena and underlying mechanisms.

References

  1. 1

    Mendel, G. Versuche über Pflanzen Hybriden. Verhandlungen des naturforschenden Vereines in Brünn 4, 3–47 (1866).

  2. 2

    Correns, C.G. Mendels Regel über das Verhalten der Nachkommenschaft der rassenbastarde. Berichte der Deutschen Botanischen Gesellschaft 18, 158–168 (1900).

  3. 3

    de Vries, H. Sur la loi de disjonction des hybrides. Comptes Rendus de l'Academie des Sciences (Paris) 130, 845–847 (1900).

  4. 4

    Tschermak, E. Über künstliche Kreuzung bei Pisum sativum. Berichte der Deutschen Botanischen Gesellschaft 18, 232–239 (1900).

  5. 5

    McClintock, B. The control of gene action in maize. Brookhaven Symp. Biol. 18, 162–184 (1965).

  6. 6

    Napoli, C., Lemieux, C. & Jorgensen, R. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous gene in trans. Plant Cell 2, 279–289 (1990).

  7. 7

    van der Krol, A.R., Mur, L.A., Beld, M., Mol, J.N.M. & Stuitje, A.R. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2: 291–299 (1990).

  8. 8

    Smith, C.J.S. et al. Expression of a truncated tomato polygalacturonase gene inhibits expression of the endogenous gene in transgenic plants. Mol. Gen. Genet. 224, 477–481 (1990).

  9. 9

    Laibach, F. Zur Frage nach der Individualität der Chromosomen in Pflanzenreich. Beih. Bot. Cbl. (1 Abt.) 22, 197–210 (1907).

  10. 10

    Laibach, F. Arabidopsis thaliana (L.) Heynh. als Objekt für genetische und entwicklungs-physiologische Untersuchungen. Bot. Arch. 44, 439–455 (1943).

  11. 11

    Langridge, J. Biochemical mutations in the crucifer Arabidopsis thaliana (L.) Heynh. Nature 76, 260–261 (1955).

  12. 12

    Redei, G.P. Supervital mutants of Arabidopsis. Genetics 47, 443–460 (1962).

  13. 13

    Leutwiler, L.S., Hough-Evans, B.R. & Meyerowitz, E.M. The DNA of Arabidopsis thaliana. Mol. Gen. Genet. 194, 15–23 (1984).

  14. 14

    Pruitt, R.E. & Meyerowitz, E.M. Characterization of the genome of Arabidopsis thaliana. J. Mol. Biol. 187, 169–183 (1986).

  15. 15

    Redei, G.P. Arabidopsis as a genetic tool. Annu. Rev. Genet. 9, 111–127 (1975).

  16. 16

    Meyerowitz, E.M. & Pruitt, R.E. Arabidopsis thaliana and plant molecular genetics. Science 229, 1214–1218 (1985).

  17. 17

    Estelle, M.A. & Somerville, C.R. The mutants of Arabidopsis. Trends Genet. 2, 89–93 (1986).

  18. 18

    Meyerowitz, E.M. Arabidopsis thaliana. Annu. Rev. Genet. 21, 93–111 (1987).

  19. 19

    The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000).

  20. 20

    Goff, S.A. et al. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296, 92–100 (2002).

  21. 21

    Yu, J. et al. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296, 79–92 (2002).

  22. 22

    Raikhel, N.V. & Minorsky, P.V. Celebrating plant diversity. Plant Phys. 127, 1325–1327 (2001).

  23. 23

    Schaefer, D.G. Gene targeting in Physcomitrella patens. Curr. Opin. Plant Biol. 4, 143–150 (2001).

  24. 24

    Chatterjee, A. & Roux, S.J. Ceratopteris richardii: a productive model for revealing secrets of signaling and development. J. Plant Growth Regul. 19, 284–289 (2002).

  25. 25

    Carpenter, R. & Coen, E.S. Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev. 4, 1483–1493 (1990).

  26. 26

    Schwarz-Sommer, Z., Huijser, P., Nacken, W., Saedler, H. & Sommer, H. Genetic control of flower development: homeotic genes of Antirrhinum majus. Science 250, 931–936 (1990).

  27. 27

    Bowman, J.L., Smyth, D.R. & Meyerowitz, E.M. Genetic interactions among floral homeotic genes of Arabidopsis. Development 112, 1–20 (1991).

  28. 28

    Sommer, H. et al. Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J. 9, 605–613 (1990).

  29. 29

    Yanofsky, M.F. et al. The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors. Nature 346, 35–40 (1990).

  30. 30

    Lewis, E.B. A gene complex controlling segmentation in Drosophila. Nature 276, 565–570 (1978).

  31. 31

    Gehring W.J. Homeo boxes in the study of development. Science 236, 1245–1252 (1987).

  32. 32

    Jack, T., Brockman, L.L. & Meyerowitz, E.M. The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS-box and is expressed in petals and stamens. Cell 68, 683–697 (1992).

  33. 33

    Goto, K. & Meyerowitz, E.M. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8, 1548–1560 (1994).

  34. 34

    Mandel, M.A. et al. Manipulation of flower structure in transgenic tobacco. Cell 71, 133–143 (1992).

  35. 35

    Tröbner, W. et al. GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J. 11, 4693–4704 (1992).

  36. 36

    Huijser, P. et al. Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO J. 11, 1239–1249 (1992).

  37. 37

    Bradley, D., Carpenter, R., Sommer, H., Hartley, N. & Coen, E. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the Plena locus of Antirrhinum. Cell 72, 85–95 (1993).

  38. 38

    Drews, G.N., Bowman, J.L. & Meyerowitz, E.M. Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65, 991–1002 (1991).

  39. 39

    Mandel, M.A., Gustafson-Brown, C., Savidge, B. & Yanofsky, M.F. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360, 273–277 (1992).

  40. 40

    Mizukami, Y. & Ma, H. Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71, 119–131 (1992).

  41. 41

    Jack, T., Fox, G.L. & Meyerowitz, E.M. Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and post-transcriptional regulation determine floral organ identity. Cell 76, 703–716 (1994).

  42. 42

    Sakai, H., Medrano, L.J. & Meyerowitz, E.M. Arabidopsis floral boundary maintenance by SUPERMAN. Nature 378, 199–203 (1995).

  43. 43

    Krizek, B.A. & Meyerowitz, E.M. The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 122, 11–22 (1996).

  44. 44

    Mandel, M.A. & Yanofsky, M.F. A gene triggering flower formation in Arabidopsis. Nature 377, 522–524 (1995).

  45. 45

    Coen, E.S. et al. Floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63, 1311–1322 (1990).

  46. 46

    Weigel, D., Alvarez, J., Smyth, D.R., Yanofsky, M.F. & Meyerowitz, E.M. LEAFY controls floral meristem identity in Arabidopsis. Cell 69, 843–859 (1992).

  47. 47

    Parcy, F., Nilsson, O., Busch, M.A., Lee, I. & Weigel, D. A genetic framework for floral patterning. Nature 395, 561–566 (1998).

  48. 48

    Busch, M.A., Bomblies, K. & Weigel, D. Activation of a floral homeotic gene in Arabidopsis. Science 285, 585–587 (1999).

  49. 49

    Wagner, D. Sablowski, R.W.M. & Meyerowitz, E.M. Transcriptional activation of APETALA1 by LEAFY. Science 285, 582–584 (1999).

  50. 50

    Ambrose, B.A. et al. Molecular and genetic analysis of the Silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol. Cell 5, 569–579 (2000).

  51. 51

    Kyozuka, J., Kobayashi, T., Morita, M. & Shimamoto, K. Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A, B and C genes. Plant Cell Physiol. 41, 710–718 (2000).

  52. 52

    Tandre, K., Svenson, M., Svensson, M.E. & Engstrom, P. Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms. Plant J. 15, 615–623 (1998).

  53. 53

    Sundstrom, J. et al. MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B-class floral homeotic genes in angiosperms. Dev. Genet. 25, 253–66 (1999).

  54. 54

    Mouradov, A. et al. DEF/GLO-like MADS-box gene from a gymnosperm: Pinus radiata contains an ortholog of angiosperm B class floral homeotic genes. Dev. Genet. 25, 245–252 (1999).

  55. 55

    Angenent, G.C., Franken, J., Busscher, M., Weiss, D. & van Tunen, A.J. Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. Plant J. 5, 33–44 (1994).

  56. 56

    Pnueli, L., Hareven, D., Broday, L., Hurwitz, C. & Lifschitz, E. The TM5 MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant Cell 6, 175–186 (1994).

  57. 57

    Pelaz, S., Ditta, G.S., Baumann, E., Wisman, E. & Yanofsky, M.F. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405, 200–203 (2000).

  58. 58

    Egea-Cortines, M., Saedler, H. & Sommer, H. Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J. 18, 5370–5379 (1999).

  59. 59

    Honma, T. & Goto, K. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409, 525–529 (2001).

  60. 60

    Pelaz, S., Tapia-Lopez, R., Alvarez-Buylla, E.R. & Yanofsky, M.F. Conversion of leaves into petals in Arabidopsis. Curr. Biol. 11, 182–184 (2001).

  61. 61

    Goethe, J.W. The Metamorphosis of Plants translated by A. Arber as Goethe's botany. Chronica Botanica 10, 67–115 (1946).

  62. 62

    Cashmore, A.R., Jarillo, J.A., Wu, Y.J. & Liu, D. Cryptochromes: blue light receptors for plants and animals. Science 284, 760–765 (1999).

  63. 63

    Quail, P.H. et al. Phytochromes: photosensory perception and signal transduction. Science 268, 675–680 (1995).

  64. 64

    Quail, P.H. The phytochrome family: dissection of functional roles and signalling pathways among family members. Phil. Trans. R. Soc. Lond. B 353, 1399–1403 (1998).

  65. 65

    Whitelam, G.C., Patel, S. & Devlin, P.F. Phytochromes and photomorphogenesis in Arabidopsis. Phil. Trans. R. Soc. Lond. B 353, 1445–1453 (1998).

  66. 66

    Briggs, W.R. & Olney, M.A. Photoreceptors in plant photomorphogenesis to date. Five phytochromes, two cryptochromes, one phototropin, and one superchrome. Plant Physiol. 125, 85–88 (2001).

  67. 67

    Neff, M.M., Fankhauser, C. & Chory, J. Light: an indicator of time and place. Genes Dev. 14, 257–271 (2000).

  68. 68

    Harmer, S.L., Panda, S. & Kay, S.A. Molecular bases of circadian rhythms. Annu. Rev. Cell. Dev. Biol. 17, 215–253 (2001).

  69. 69

    McClung, C.R., Salomé, P.A. & Michael, T.P. The Arabidopsis circadian system. In The Arabidopsis Book online <http://www.aspb.org/publications/arabidopsis/> (eds. Somerville, C.R. & Meyerowitz, E.M.) (ASPB, Rockville, USA, 2002). doi/10.1199/tab.0044.

  70. 70

    Koornneef, M., Rolff, E. & Spruit, C.J.P. Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (l.) Heynh. Z. Pflanzenphysiol. 100, 147–160 (1980).

  71. 71

    Ahmad, M. & Cashmore, A.R. HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366, 162–166 (1993).

  72. 72

    Ahmad, M., Jarillo, J.A., Smirnova, O. & Cashmore, A.R. The CRY1 blue light photoreceptor of Arabidopsis interacts with phytochrome A in vitro. Mol. Cell 1, 939–948 (1998).

  73. 73

    Más, P., Devlin, P.F., Panda, S. & Kay, S.A. Functional interaction of phytochrome B and cryptochrome 2. Nature 408, 207–211 (2000).

  74. 74

    Ahmad, M., Jarillo, J.A., Smirnova, O & Cashmore, A.R. Cryptochrome blue-light photoreceptors of Arabidopsis implicated in phototropism. Nature 392, 720–723 (1998).

  75. 75

    Stanewsky, R. et al. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95, 681–692 (1998).

  76. 76

    Kume, K. et al. MCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98, 193–205 (1999).

  77. 77

    Muramoto, T., Kohchi, T., Yokota, A., Hwang, I. & Goodman H.M. The Arabidopsis photomorphogenic mutant hy1 is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell 11, 335–347 (1999).

  78. 78

    Kohchi, T. et al. The Arabidopsis HY2 gene encodes phytochromobilin synthase, a ferredoxin-dependent biliverdin reductase. Plant Cell 13, 425–436 (2001).

  79. 79

    Reed, J.W., Nagpal, P., Poole, D.S., Furuya, M. & Chory, J. Mutations in the gene for the red far-red light receptor phytochrome-B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5, 147–157 (1993).

  80. 80

    Devlin, P.F., Patel, S.R. & Whitelam, G.C. Phytochrome E influences internode elongation and flowering time in Arabidopsis. Plant Cell 10, 1479–1487 (1998).

  81. 81

    Aukerman, M.J. et al. A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing. Plant Cell 9, 1317–1326 (1997).

  82. 82

    Dehesh, K. et al. Arabidopsis Hy8 locus encodes phytochrome-A. Plant Cell 5, 1081–1088 (1993).

  83. 83

    Whitelam, G.C. et al. Phytochrome-A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 5, 757–768 (1993).

  84. 84

    Koornneef, M. & Kendrick, R.E. Photomorphogenic mutants of higher plants. In Photomorphogenesis in Plants (eds. Kendrick, R.E. & Kronenberg, G.H.M.) 601–628 (Kluwer Academic, Dordrecht, 1994).

  85. 85

    Ni, M., Tepperman, J.M. & Quail, P.H. PIF3, a phytochrome interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95, 657–667 (1998).

  86. 86

    Kircher, S. et al. Light quality-dependent nuclear import of the plant photoreceptors phytochrome A and B. Plant Cell 11, 1445–1456 (1999).

  87. 87

    Ni, M., Tepperman, J.M. & Quail, P.H. Binding of phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light. Nature 400, 781–784 (1999).

  88. 88

    Yeh, K.-C. & Lagarias, J.C. Eukaryotic phytochromes: light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc. Natl. Acad. Sci. USA 95, 13976–13981 (1998).

  89. 89

    Yeh, K.C., Wu, S.H., Murphy, J.T. & Lagarias, J.C. A cyanobacterial phytochrome two component light regulatory sensory system. Science 277, 1505–1508 (1997).

  90. 90

    Fankhauser, C. et al. PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. Science 284, 1539–1541 (1999).

  91. 91

    Chory, J., Peto, C., Feinbaum, R., Pratt, L. & Ausubel, F. Arabidopsis thaliana mutant that develops as a light-grown plant in the absence of light. Cell 58, 991–999 (1989).

  92. 92

    Deng, X.W., Caspar, T. & Quail, P.H. Cop1—a regulatory locus involved in light-controlled development and gene expression in Arabidopsis. Genes Dev. 5, 1172–1182 (1991).

  93. 93

    Deng, X.W. & Quail, P.H. Signalling in light-controlled development. Semin. Cell Dev. Biol. 10, 121–129 (1999).

  94. 94

    Wei, N. et al. The COP9 complex is conserved between plants and mammals and is related to the 26S proteasome regulatory complex. Curr. Biol. 8, 919–922 (1998).

  95. 95

    Osterlund, M.T., Hardtke, C.S., Wei, N. & Deng, X.-W. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405, 462–466 (2000).

  96. 96

    Oyama, T., Shimura, Y., & Okada, K. The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev. 11, 2983–2995 (1997).

  97. 97

    Chattopadhyay, S. et al. Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10, 673–683 (1998).

  98. 98

    Ang, L.H. et al. Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol. Cell 1, 213–222 (1998).

  99. 99

    Wang, H., Ma, L.G., Li, J.M., Zhao, H.Y. & Deng, X.-W. Direct interaction of Arabidopsis cryptochromes with COP1 in light control development. Science 294, 154–158 (2001).

  100. 100

    Briggs, W.R. & Christie, J.M. Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci. 7, 204–210 (2002).

  101. 101

    Liscum, E. & Briggs, W.R. Mutations in the NPH1 locus disrupt the perception of phototropic stimuli. Plant Cell 7, 473–485 (1995).

  102. 102

    Huala, E. et al. Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278, 2120–2123 (1997).

  103. 103

    Christie, J.M. et al. Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282, 1698–1701 (1998).

  104. 104

    Kagawa, T. et al. Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291, 2138–2141 (2001).

  105. 105

    Sakai, T. et al. Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc. Natl. Acad. Sci. USA 98, 6969–6974 (2001).

  106. 106

    Moore-Ede, C.M., Sulzman, F.M. & Fuller, C.A. The Clocks That Time Us (Harvard Univ. Press, Cambridge, MA) (1982).

  107. 107

    Harmer, S.L. et al. Orchestarted transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110–2113 (2000).

  108. 108

    Schaffer, R. et al. Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13, 113–123 (2001).

  109. 109

    Bagnall, D.J. & King, R.W. Phytochrome, photosynthesis and flowering of Arabidopsis thaliana: photophysiological studies using mutants and transgenic lines. Aust. J. Plant Physiol. 28, 401–408 (2001).

  110. 110

    Pineiro, M. & Coupland, G. The control of flowering time and floral identity in Arabidopsis. Plant Physiol. 117, 1–8 (1998).

  111. 111

    Coupland, G. Regulation of flowering by photoperiod in Arabidopsis. Plant Cell Environ. 20, 785–789 (1997).

  112. 112

    Amasino, R.M. Control of flowering time in plants. Curr. Opin. Genet. Dev. 6, 480–487 (1996).

  113. 113

    Somers, D.E., Delvin, P.F. & Kay, S.A. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 282, 1488–1490 (1998).

  114. 114

    Guo, H., Yang, H., Mockler, T.C. & Lin, C. Regulation of flowering time by Arabidopsis photoreceptors. Science 279, 1360–1363 (1998).

  115. 115

    Koornneef, M., Hanhart, C.J. & van der Veen, J.H. A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol. Gen. Genet. 229, 57–66 (1991).

  116. 116

    Hicks, K.A. et al. Conditional circadian dysfunction of the Arabidopsis early-flowering3 mutant. Science 274, 790–792 (1996).

  117. 117

    Schaffer, R. et al. LATE ELONGATED HYPOCOTYL, an Arabidopsis gene encoding a MYB transcription factor, regulates circadian rhythmicity and photoperiodic responses. Cell 93, 1219–1229 (1998).

  118. 118

    Wang, Z. & Tobin, E.M. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93, 1207–1217 (1998).

  119. 119

    Fowler, S. et al. GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J. 18, 4679–4688 (1999).

  120. 120

    Park, D.H. et al. Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285, 1579–1582 (1999).

  121. 121

    Súarez-López, P. et al. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410, 1116–1120 (2001).

  122. 122

    Bünning, E. Die endogene tagesrhythmik als grundlage der photoperiodischen reaktion. Ber. Dtsch. Bot. Ges. 54, 590–607 (1936).

  123. 123

    Flor, H.H. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9, 275–296 (1971).

  124. 124

    Rossi, M. et al. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. USA 95, 9750–9754 (1998).

  125. 125

    Ellis, J., Dodds, P. & Pryor, T. Structure, function and evolution of plant disease resistance genes. Curr. Opin. Plant Biol. 3, 278–284 (2000).

  126. 126

    Dangl, J.L. & Jones, J.D. Plant pathogens and integrated defence responses to infection. Nature 411, 826–833 (2001).

  127. 127

    van der Biezen, E.A. & Jones, J.D. Plant disease–resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23, 454–456 (1998).

  128. 128

    Mackey, D., Holt, B.F., Wiig, A. & Dangl, J.L. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743–754 (2002).

  129. 129

    Kruger, J. et al. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296, 744–747 (2002).

  130. 130

    Kim, Y.J., Lin, N.-C. & Martin, G.B. Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109, 589–598 (2002).

  131. 131

    Shao, F., Merritt, P.M., Bao, Z., Innes, R.W. & Dixon, J.E. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109, 575–588 (2002).

  132. 132

    Schneider, D.S. Plant immunity and film noir: what gumshoe detectives can teach us about plant-pathogen interactions. Cell 109, 537–540 (2002).

  133. 133

    Century, K.S., Holub, E.B. & Staskawicz, B.J. NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc. Natl. Acad. Sci. USA 92, 6597–6601 (1995).

  134. 134

    Parker, J.E. et al. Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8, 2033–2046 (1996).

  135. 135

    Aarts, N. et al. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene–mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. USA 95, 10306–10311 (1998).

  136. 136

    Xiao, S. et al. Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291, 118–120 (2001).

  137. 137

    Noël, L. et al. Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11, 2099–2111 (1999).

  138. 138

    Galton, F. Natural Inheritance (Macmillan, London, 1889).

  139. 139

    Fisher, R.A. The correlation between relatives on the supposition of Mendelian inheritance. Trans. R. Soc. Edinb. 52, 399–433 (1918).

  140. 140

    Wright, S. The method of path coefficients. Ann. Math. Stat. 5, 161–215 (1934).

  141. 141

    Mather, K. Biometrical Genetics (Methuen, London, 1949).

  142. 142

    Mackay, T.F. The genetic architecture of quantitative traits. Annu. Rev. Genet. 35, 303–339 (2001).

  143. 143

    Thoday, J.M. Location of polygenes. Nature 191, 368–370 (1961).

  144. 144

    Lander, E.S. & Botstein, D. Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121, 185–199 (1989).

  145. 145

    Doerge, R.W. Mapping and analysis of quantitative trait loci in experimental populations. Nat. Rev. Genet. 3, 43–52 (2002).

  146. 146

    Koornneef, M., Blankestijn-de Vries, H., Hanhart, C., Soope, W. & Peeters, T. The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type. Plant J. 6, 911–919 (1994).

  147. 147

    Lee, I., Michaels, S.D., Masshardt, A.S. & Amasino, R.M. The late-flowering phenotype of FRIGIDA and mutations in LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J. 6, 903–909 (1994).

  148. 148

    Doebley, J. & Stec, A. Genetic analysis of the morphological differences between maize and teosinte. Genetics 129, 285–295 (1991).

  149. 149

    Doebley, J. & Stec, A. Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. Genetics 134, 559–570 (1993).

  150. 150

    Doebley, J., Stec, A. & Gustus, C. teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141, 333–346 (1995).

  151. 151

    Doebley, J., Stec, A. & Hubbard, L. The evolution of apical dominance in maize. Nature 386, 485–488 (1997).

  152. 152

    Eshed, Y. & Zamir, D. An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141, 1147–1162 (1995).

  153. 153

    Fridman, E., Pleban, T. & Zamir, D. A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proc. Natl. Acad. Sci. USA 97, 4718–4723 (2000).

  154. 154

    Frary, A. et al. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289, 85–88 (2000).

  155. 155

    Takahashi, A., Tsaur, S-C., Coyne J.A. & Wu, C-I. The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 98, 3920–3925 (2001).

  156. 156

    El-Din El-Assal, S., Alonso-Blanco, C., Peeters, A.J., Raz, V. & Koornneef, M. A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat. Genet. 29, 435–440 (2001).

  157. 157

    Maloof, J.N. et al. Natural variation in light sensitivity of Arabidopsis. Nat. Genet. 29, 441–446 (2001).

  158. 158

    Alonso-Blanco, C. & Koornneef, M. Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. Trends Plant Sci. 5, 22–29 (2000).

  159. 159

    Yano, M., Kojima, S., Takahashi, Y., Lin, H. & Sasaki, T. Genetic control of flowering time in rice, a short-day plant. Plant Physiol 127, 1425–1429 (2001).

  160. 160

    Zamir, D. Improving plant breeding with exotic genetic libraries. Nat. Rev. Genet. 2, 983–989 (2001).

  161. 161

    Dudash, M.R. & Carr, D.E. Genetics underlying inbreeding depression in Mimulus with contrasting mating systems. Nature 393, 682–684 (1998).

  162. 162

    Li, Z.K. et al. Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. Genetics 158, 1737–1753 (2001).

  163. 163

    Luo, L.J. et al. Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. II. Grain yield components. Genetics 158, 1755–1771 (2001).

  164. 164

    Harushima, Y., Nakagahra, M., Yano, M., Sasaki, T. & Kurata, N. Diverse variation of reproductive barriers in three intraspecific rice crosses. Genetics 160, 313–322 (2002).

  165. 165

    Schemske, D.W. & Bradshaw, H.D., Jr. Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc. Natl. Acad. Sci. USA 96, 11910–11915 (1999).

  166. 166

    Hageman, R. Somatische konversion bei Lycopersicon esculentum Mill. Z. Vererbungslehre 89, 587–613 (1958).

  167. 167

    Brink, R.A. Paramutation at the R locus in maize. Cold Spring Harbor Symp. Quant. Biol. 23, 379–391 (1958).

  168. 168

    Kermicle, J.L. Dependence of the R-mottled aleurone phenotype in maize on mode of sexual transmission. Genetics 66, 69–85 (1970).

  169. 169

    Mittelsten Scheid, O. & Paszkowski, J. Transcriptional gene silencing mutants. Plant Mol. Biol. 43, 235–241 (2000).

  170. 170

    Morel, J.B. & Vaucheret, H. Post-transcriptional gene silencing mutants. Plant Mol. Biol. 43, 275–284 (2000).

  171. 171

    Finnegan, E.J. & Kovac, K.A. Plant DNA methyltransferases. Plant Mol. Biol. 43, 189–201 (2000).

  172. 172

    Martienssen, R.A. & Colot, V. DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293, 1070–1074 (2001).

  173. 173

    Vongs, A., Kakutani, T., Martienssen, R.A. & Richards, E.J. Arabidopsis thaliana DNA methylation mutants. Science 260, 1926–1928 (1993).

  174. 174

    Mittelsten Scheid, O., Afsar, K. & Paszkowski, J. Release of epigenetic gene silencing by trans-acting mutations in Arabidopsis. Proc. Natl. Acad. Sci. U S A. 95, 632–637 (1998).

  175. 175

    Bartee, L., Malagnac, F. & Bender, J. Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev. 15, 1753–1758 (2001).

  176. 176

    Lindroth, A.M. et al. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292, 2077–2080 (2001).

  177. 177

    Jackson, J.P., Lindroth, A.M., Cao, X. & Jacobsen, S.E. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416, 556–560 (2002).

  178. 178

    Malagnac, F., Bartee, L. & Bender, J. An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J. 21, 6842–6852 (2002).

  179. 179

    Russo, V.E.A., Martiessen, R.A. & Riggs, A.D. (eds.) Epigenetic Mechanisms of Gene Regulation (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1996).

  180. 180

    Matzke, M. & Matzke, A. Special issue: epigenetics. Plant Mol. Biol. 43, 121–415 (2000).

  181. 181

    Riddihough, G. & Pennisi, E. The evolution of epigenetics. Science 293, 1063–1102 (2001).

  182. 182

    Dunlap, J.C. & Wu, C.-T. (eds.). Homology effects. Adv. Genet. 46 (2002) (Academic Press, San Diego, 2002).

  183. 183

    Matzke, M., Matzke, A.J. & Kooter, J.M. RNA: guiding gene silencing. Science 293, 1080–1083 (2001).

  184. 184

    Hamilton AJ, Baulcombe DC . A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950–952 (1999).

  185. 185

    Baulcombe, D. RNA silencing. Curr. Biol. 12, 82–84 (2002).

  186. 186

    Palauqui J.C., Elmayan, T., Pollien, J.M. & Vaucheret, H. Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J. 16, 4738–4745 (1997).

  187. 187

    Voinnet O. & Baulcombe DC. Systemic signalling in gene silencing. Nature 389, 553 (1997).

  188. 188

    Jorgensen, R.A., Atkinson, R.G., Forster, R.L. & Lucas, W.J. An RNA-based information superhighway in plants. Science 279, 1486–1487 (1998).

  189. 189

    Orlando, V. & Paro, R. Chromatin multiprotein complexes involved in the maintenance of transcription patterns. Curr. Opin. Genet. Dev. 5, 174–179 (1995).

  190. 190

    Pirrotta, V. Chromatin complexes regulating gene expression in Drosophila. Curr. Opin. Genet. Dev. 5, 466–472 (1995).

  191. 191

    Brock, H.W. & van Lohuizen, M. The Polycomb group—no longer an exclusive club? Curr. Opin. Genet. Dev. 11, 175–181 (2001).

  192. 192

    Köhler C. & Grossniklaus, U. Epigenetic inheritance of expression states in plant development: the role of Polycomb group proteins. Curr. Opin. Cell Biol. 14, 773–779 (2002).

  193. 193

    Goodrich, J. et al. A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386, 44–51 (1997).

  194. 194

    van Lohuizen, M. The trithorax-group and polycomb-group chromatin modifiers: implications for disease. Curr. Opin. Genet. Dev. 9, 355–361 (1999).

  195. 195

    Grossniklaus, U., Vielle-Calzada J.-P, Hoeppner, M.A. & Gagliano, W.B. Maternal control of embryogenesis by MEDEA, a Polycomb group gene in Arabidopsis. Science 280, 446–450 (1998).

  196. 196

    Ohad, N. et al. Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization. Plant Cell 11, 407–16 (1999).

  197. 197

    Luo, M. et al. Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96, 296–301 (1999).

  198. 198

    Grossniklaus, U., Spillane, C., Page, D.R. & Köhler, C. Genomic imprinting and seed development: endosperm formation with and without sex. Curr. Opin. Plant Biol. 4, 21–27 (2001).

  199. 199

    Gendall, A.R., Levy, Y.Y., Wilson, A. & Dean, C. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107, 525–535 (2001).

  200. 200

    Meyerowitz, E.M. Plants compared to animals: the broadest comparative study of development. Science 295, 1482–1485 (2002).

  201. 201

    Matzke, M.A., Aufsatz, W., Kanno, T, Mette, M.F. & Matzke, A.J. Homology-dependent gene silencing and host defense in plants. Adv. Genet. 46, 235–275 (2002).

  202. 202

    Winzeler, E.A. et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901–906 (1999).

  203. 203

    Tong, A.H. et al. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294, 2364–2368 (2001).

  204. 204

    Jorgensen, P., Nishikawa, J.L., Breitkreutz, B.J. & Tyers, M. Systematic identification of pathways that couple cell growth and division in yeast. Science 297, 395–400 (2002).

  205. 205

    Giaever, G. et al. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387–91 (2002).

  206. 206

    Kempin, S.A., Savidge, B. & Yanofsky, M.F. Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267, 522–525 (1995).

  207. 207

    Page, D.R. & Grossniklaus, U. The art and design of genetic screens: Arabidopsis thaliana. Nat. Rev. Genet. 3, 124–136 (2002).

  208. 208

    Weigel, D. et al. Activation tagging in Arabidopsis. Plant Physiol. 122, 1003–1013 (2000).

  209. 209

    Li, Y., Wu, Y.H., McAvoy, R. & Duan, H. Transgenics in crops. Biotechnol. Annu. Rev. 7, 239–260 (2001).

  210. 210

    Ye, X. et al. Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287, 303–305 (2000).

  211. 211

    Potrykus I. Golden rice and beyond. Plant Physiol. 125, 1157–1161 (2001).

  212. 212

    Alvarez, J. & Smyth, D.R. CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126, 2377–2386 (1999).

  213. 213

    Ng, M. & Yanofsky, M.F. Activation of the Arabidopsis B class homeotic genes by APETALA1. Plant Cell 13, 739–753 (2001).

  214. 214

    Lohmann, J.U. et al. A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell. 105, 793–803 (2001).

  215. 215

    Lamb, R.S., Hill, T.A., Tan, Q.K.-G. & Irish, V.F. Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 129, 2079–2086 (2002).

  216. 216

    Samach, A. et al. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613–1616 (2000).

  217. 217

    Simpson, G.G. & Dean, C. Arabidopsis, the Rosetta stone of flowering time? Science 296, 285–289 (2002).

  218. 218

    Alonso-Blanco, C., El-Assal, S.E.-D., Coupland, G. & Koornneef, M. Analysis of natural variation at flowering time loci in the Landsberg erecta and Cape Verde Island ecotypes of Arabidopsis thaliana. Genetics 149, 749–764 (1998).

  219. 219

    Schauer, S.E., Jacobsen, S.E., Meinke, D.W. & Ray, A. DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci. 7, 487–491 (2002).

  220. 220

    Anandalakshmi R. et al. A viral suppressor of gene silencing in plants. Proc. Natl. Acad. Sci. USA 95, 13079–13084 (1998).

  221. 221

    Liscum, E. Phototropism: mechanisms and outcomes. In The Arabidopsis Book online <http://www.aspb.org/publications/arabidopsis/> (eds. Somerville, C.R. & Meyerowitz, E.M. (ASPB, Rockville, 2002). doi/10.1199/tab.0042.

Download references

Acknowledgements

We apologize to colleagues whose research areas we could not cover. We thank J. Banks, C. Chapple, S. Curtis, R. Dudler, Y. Eshed, S. Goodwin, M. Green, M. Koornneef, C. Lagarias, S. Lolle, S. Scofield, D. Smyth and J.-R. Xu for critically reading the manuscript.

Author information

Correspondence to Ueli Grossniklaus.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pruitt, R., Bowman, J. & Grossniklaus, U. Plant genetics: a decade of integration. Nat Genet 33, 294–304 (2003) doi:10.1038/ng1108

Download citation

Further reading