Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana

K. Schneitz; M. Hulskamp; S.D. Kopczak; R.E. Pruitt

Summary

Understanding organogenesis remains a major challenge in biology. Specification, initiation, pattern formation and cellular morphogenesis, have to be integrated to generate the final three-dimensional architecture of a multicellular organ. To tackle this problem we have chosen the ovules of the flowering plant Arabidopsis thaliana as a model system. In a first step towards a functional analysis of ovule development, we performed a large-scale genetic screen and isolated a number of sterile mutants with aberrant ovule development, We provide indirect genetic evidence for the existence of proximal-distal pattern formation in the Arabidopsis ovule primordium. The analysis of the mutants has identified genes that act at an intermediate regulatory level and control initiation of morphogenesis in response to proximal-distal patterning. A second group of genes functions at a subordinate control level and regulates general cellular processes of morphogenesis. A large group of male and female sterile mutants shows defects restricted to early or late gametogenesis. In addition, we propose that the mature ovule obtains its overall curved shape by at least three different processes that act in only one domain of the ovule.

REFERENCES

1. Angenent G. C.,
2. Franken J.,
3. Busscher M.,
4. van Dijken A.,
5. van Went J. L.,
6. Dons H. J. M.,
7. van Tunen A. J.
(1995) A novel class of MADS box genes is involved in ovule development in Petunia. Plant Cell 7, 1569–1582
OpenUrl Abstract/FREE Full Text
1. Benavante R. S.,
2. Skorupska H.,
3. Palmer R. G.,
4. Shoemaker R.
(1989) Embryo sac development in the cv. ks male sterile, female sterile line of soybean (Glycine max). Amer. J. Bot 76, 1759–1768
OpenUrl CrossRef
1. Bowman J. L.,
2. Sakai H.,
3. Jack T.,
4. Weigel D.,
5. Mayer U.,
6. Meyerowitz E. M.
(1992) SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114, 599–615
OpenUrl Abstract
1. Coen E. S.,
2. Meyerowitz E. M.
(1991) The war of the whorls: genetic interactions controlling flower development. Nature 353, 31–37
OpenUrl CrossRef PubMed Web of Science
1. Colombo L.,
2. Franken J.,
3. Koetje E.,
4. van Went J.,
5. Dons H. J. M.,
6. Angenent G. C.,
7. van Tunen A. J.
(1995) The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7, 1859–1868
OpenUrl Abstract/FREE Full Text
1. Elliott R. C.,
2. Betzner A. S.,
3. Huttner E.,
4. Oakes M. P.,
5. Tucker W. Q. J.,
6. Gerentes D.,
7. Perez P.,
8. Smyth D. R.
(1996) AINTEGUMENTA, an APETALA2 -like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8, 155–168
OpenUrl Abstract/FREE Full Text
1. Evans P. T.,
2. Malmberg R. L.
(1989) Alternative pathways of tobacco placental development: time of commitment and analysis of a mutant. Dev. Biol 136, 273–283
OpenUrl CrossRef PubMed Web of Science
1. Gaiser J. C.,
2. Robinson-Beers K.,
3. Gasser C. S.
(1995) The Arabidopsis SUPERMAN gene mediates asymmetric growth of the outer integument of ovules. Plant Cell 7, 333–345
OpenUrl Abstract/FREE Full Text
1. Huang B.-Q.,
2. Sheridan W. F.
(1996) Embryo sac development in the maize indeterminate gametophyte1 mutant: abnormal nuclear behavior and defective microtubule organization. Plant Cell 8, 1391–1407
OpenUrl Abstract/FREE Full Text
1. Hulskamp M.,
2. Schneitz K.,
3. Pruitt R. E.
(1995) Genetic evidence for a long range activity that directs pollen tube guidance in Arabidopsis. Plant Cell 7, 57–64
OpenUrl Abstract/FREE Full Text
1. Jofuku K. D.,
2. den Boer B. G. W.,
3. Van Montagu M.,
4. Okamuro J. K.
(1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6, 1211–1225
OpenUrl Abstract/FREE Full Text
1. Kennell J. C.,
2. Horner H. T.
(1985) Influence of the soybean male-sterile gene (ms1) on the development of the female gametophyte. Can. J. Genet. Cytol 27, 200–209
OpenUrl
1. Kermicle J. L.
(1971) Pleiotropic effects on seed development of the indeterminate gametophyte gene in maize. Amer. J. Bot 58, 1–7
OpenUrl CrossRef Web of Science
1. Klucher K. M.,
2. Chow H.,
3. Reiser L.,
4. Fischer R. L.
(1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8, 137–153
OpenUrl Abstract/FREE Full Text
1. Lang J. D.,
2. Ray S.,
3. Ray A.
(1994) sin1, a mutation affecting female fertility in Arabidopsis, interacts with mod1, its recessive modifier. Genetics 137, 1101–1110
OpenUrl Abstract/FREE Full Text
1. Leon-Kloosterziel K. M.,
2. Keijzer C. J.,
3. Koornneef M.
(1994) A seed shape mutant of Arabidopsis that is affected in integument development. Plant Cell 6, 385–392
OpenUrl Abstract/FREE Full Text
1. Lin B.-Y.
(1978) Structural modifications of the female gametophyte associated with the indeterminate gametophyte (ig) mutant in maize. Can. J. Genet. Cytol 20, 249–257
OpenUrl CrossRef
1. Liu Z.,
2. Meyerowitz E. M.
(1995) LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121, 975–991
OpenUrl Abstract
1. Ma H.
(1994) The unfolding drama of flower development: recent results from genetic and molecular analyses. Genes Dev 8, 745–756
OpenUrl FREE Full Text
1. Ma H.,
2. Yanofsky M. F.,
3. Meyerowitz E. M.
(1991) AGL1 - ALG6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev 5, 484–495
OpenUrl Abstract/FREE Full Text
1. Mansfield S. G.,
2. Briarty L. G.,
3. Erni S.
(1991) Early embryogenesis in Arabidopsis thaliana. I. The mature embryo sac. Can. J. Bot 69, 447–460
OpenUrl CrossRef Web of Science
1. Mayer U.,
2. Torres Ruiz R. A.,
3. Berleth T.,
4. Misera S.,
5. Jurgens G.
(1991) Mutations affecting body organization in the Arabidopsis embryo. Nature 353, 402–407
OpenUrl CrossRef
1. Modrusan Z.,
2. Reiser L.,
3. Feldmann K. A.,
4. Fischer R. L.,
5. Haughn G. W.
(1994) Homeotic transformation of ovules into carpel-like structures in Arabidopsis. Plant Cell 6, 333–349
OpenUrl Abstract/FREE Full Text
1. Ray A.,
2. Robinson-Beers K.,
3. Ray S.,
4. Baker S. C.,
5. Lang J. D.,
6. Preuss D.,
7. Milligan S. B.,
8. Gasser C. S.
(1994) Arabidopsis floral homeotic gene BELL (BEL1) controls ovule development through negative regulation of AGAMOUS gene (AG). Proc. Natl. Acad. Sci. USA 91, 5761–5765
OpenUrl Abstract/FREE Full Text
1. Reiser L.,
2. Fischer R. L.
(1993) The ovule and the embryo sac. Plant Cell 5, 1291–1301
OpenUrl FREE Full Text
1. Reiser L.,
2. Modrusan Z. L. M.,
3. Samach A.,
4. Ohad N.,
5. Haughn G. W.,
6. Fischer R. L.
(1995) The BELL1 gene encodes a homeodomain protein involved in pattern formation in the Arabidopsis ovule primordium. Cell 83, 735–742
OpenUrl CrossRef PubMed Web of Science
1. Robinson-Beers K.,
2. Pruitt R. E.,
3. Gasser C. S.
(1992) Ovule development in wild-type Arabidopsis and two female-sterile mutants. Plant Cell 4, 1237–1249
OpenUrl Abstract/FREE Full Text
1. Rounsley S. D.,
2. Ditta G. S.,
3. Yanofsky M. F.
(1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7, 1259–1269
OpenUrl Abstract/FREE Full Text
1. Sakai H.,
2. Medrano L. J.,
3. Meyerowitz E. M.
(1995) Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378, 199–203
OpenUrl CrossRef PubMed Web of Science
1. Savidge B.,
2. Rounsley S. D.,
3. Yanofsky M.
(1995) Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 7, 721–733
OpenUrl Abstract/FREE Full Text
1. Schneitz K.,
2. Hulskamp M.,
3. Pruitt R. E.
(1995) Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J 7, 731–749
OpenUrl CrossRef Web of Science
1. Weigel D.
(1995) The APETALA2 domain is related to a novel type of DNA binding domain. Plant Cell 7, 388–389
OpenUrl FREE Full Text
1. Weigel D.,
2. Meyerowitz E. M.
(1994) The abcs of floral homeotic genes. Cell 78, 203–209
OpenUrl CrossRef PubMed Web of Science

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[1] Angenent G. C.,
Franken J.,
Busscher M.,
van Dijken A.,
van Went J. L.,
Dons H. J. M.,
van Tunen A. J.
(1995) A novel class of MADS box genes is involved in ovule development in Petunia. Plant Cell 7, 1569–1582
OpenUrl Abstract/FREE Full Text

[2] Angenent G. C.,

[3] Franken J.,

[4] Busscher M.,

[5] van Dijken A.,

[6] van Went J. L.,

[7] Dons H. J. M.,

[8] van Tunen A. J.

[9] Benavante R. S.,
Skorupska H.,
Palmer R. G.,
Shoemaker R.
(1989) Embryo sac development in the cv. ks male sterile, female sterile line of soybean (Glycine max). Amer. J. Bot 76, 1759–1768
OpenUrl CrossRef

[10] Benavante R. S.,

[11] Skorupska H.,

[12] Palmer R. G.,

[13] Shoemaker R.

[14] Bowman J. L.,
Sakai H.,
Jack T.,
Weigel D.,
Mayer U.,
Meyerowitz E. M.
(1992) SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114, 599–615
OpenUrl Abstract

[15] Bowman J. L.,

[16] Sakai H.,

[17] Jack T.,

[18] Weigel D.,

[19] Mayer U.,

[20] Meyerowitz E. M.

[21] Coen E. S.,
Meyerowitz E. M.
(1991) The war of the whorls: genetic interactions controlling flower development. Nature 353, 31–37
OpenUrl CrossRef PubMed Web of Science

[22] Coen E. S.,

[23] Meyerowitz E. M.

[24] Colombo L.,
Franken J.,
Koetje E.,
van Went J.,
Dons H. J. M.,
Angenent G. C.,
van Tunen A. J.
(1995) The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7, 1859–1868
OpenUrl Abstract/FREE Full Text

[25] Colombo L.,

[26] Franken J.,

[27] Koetje E.,

[28] van Went J.,

[29] Dons H. J. M.,

[30] Angenent G. C.,

[31] van Tunen A. J.

[32] Elliott R. C.,
Betzner A. S.,
Huttner E.,
Oakes M. P.,
Tucker W. Q. J.,
Gerentes D.,
Perez P.,
Smyth D. R.
(1996) AINTEGUMENTA, an APETALA2 -like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8, 155–168
OpenUrl Abstract/FREE Full Text

[33] Elliott R. C.,

[34] Betzner A. S.,

[35] Huttner E.,

[36] Oakes M. P.,

[37] Tucker W. Q. J.,

[38] Gerentes D.,

[39] Perez P.,

[40] Smyth D. R.

[41] Evans P. T.,
Malmberg R. L.
(1989) Alternative pathways of tobacco placental development: time of commitment and analysis of a mutant. Dev. Biol 136, 273–283
OpenUrl CrossRef PubMed Web of Science

[42] Evans P. T.,

[43] Malmberg R. L.

[44] Gaiser J. C.,
Robinson-Beers K.,
Gasser C. S.
(1995) The Arabidopsis SUPERMAN gene mediates asymmetric growth of the outer integument of ovules. Plant Cell 7, 333–345
OpenUrl Abstract/FREE Full Text

[45] Gaiser J. C.,

[46] Robinson-Beers K.,

[47] Gasser C. S.

[48] Huang B.-Q.,
Sheridan W. F.
(1996) Embryo sac development in the maize indeterminate gametophyte1 mutant: abnormal nuclear behavior and defective microtubule organization. Plant Cell 8, 1391–1407
OpenUrl Abstract/FREE Full Text

[49] Huang B.-Q.,

[50] Sheridan W. F.

[51] Hulskamp M.,
Schneitz K.,
Pruitt R. E.
(1995) Genetic evidence for a long range activity that directs pollen tube guidance in Arabidopsis. Plant Cell 7, 57–64
OpenUrl Abstract/FREE Full Text

[52] Hulskamp M.,

[53] Schneitz K.,

[54] Pruitt R. E.

[55] Jofuku K. D.,
den Boer B. G. W.,
Van Montagu M.,
Okamuro J. K.
(1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6, 1211–1225
OpenUrl Abstract/FREE Full Text

[56] Jofuku K. D.,

[57] den Boer B. G. W.,

[58] Van Montagu M.,

[59] Okamuro J. K.

[60] Kennell J. C.,
Horner H. T.
(1985) Influence of the soybean male-sterile gene (ms1) on the development of the female gametophyte. Can. J. Genet. Cytol 27, 200–209
OpenUrl

[61] Kennell J. C.,

[62] Horner H. T.

[63] Kermicle J. L.
(1971) Pleiotropic effects on seed development of the indeterminate gametophyte gene in maize. Amer. J. Bot 58, 1–7
OpenUrl CrossRef Web of Science

[64] Kermicle J. L.

[65] Klucher K. M.,
Chow H.,
Reiser L.,
Fischer R. L.
(1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8, 137–153
OpenUrl Abstract/FREE Full Text

[66] Klucher K. M.,

[67] Chow H.,

[68] Reiser L.,

[69] Fischer R. L.

[70] Lang J. D.,
Ray S.,
Ray A.
(1994) sin1, a mutation affecting female fertility in Arabidopsis, interacts with mod1, its recessive modifier. Genetics 137, 1101–1110
OpenUrl Abstract/FREE Full Text

[71] Lang J. D.,

[72] Ray S.,

[73] Ray A.

[74] Leon-Kloosterziel K. M.,
Keijzer C. J.,
Koornneef M.
(1994) A seed shape mutant of Arabidopsis that is affected in integument development. Plant Cell 6, 385–392
OpenUrl Abstract/FREE Full Text

[75] Leon-Kloosterziel K. M.,

[76] Keijzer C. J.,

[77] Koornneef M.

[78] Lin B.-Y.
(1978) Structural modifications of the female gametophyte associated with the indeterminate gametophyte (ig) mutant in maize. Can. J. Genet. Cytol 20, 249–257
OpenUrl CrossRef

[79] Lin B.-Y.

[80] Liu Z.,
Meyerowitz E. M.
(1995) LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121, 975–991
OpenUrl Abstract

[81] Liu Z.,

[82] Meyerowitz E. M.

[83] Ma H.
(1994) The unfolding drama of flower development: recent results from genetic and molecular analyses. Genes Dev 8, 745–756
OpenUrl FREE Full Text

[84] Ma H.

[85] Ma H.,
Yanofsky M. F.,
Meyerowitz E. M.
(1991) AGL1 - ALG6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev 5, 484–495
OpenUrl Abstract/FREE Full Text

[86] Ma H.,

[87] Yanofsky M. F.,

[88] Meyerowitz E. M.

[89] Mansfield S. G.,
Briarty L. G.,
Erni S.
(1991) Early embryogenesis in Arabidopsis thaliana. I. The mature embryo sac. Can. J. Bot 69, 447–460
OpenUrl CrossRef Web of Science

[90] Mansfield S. G.,

[91] Briarty L. G.,

[92] Erni S.

[93] Mayer U.,
Torres Ruiz R. A.,
Berleth T.,
Misera S.,
Jurgens G.
(1991) Mutations affecting body organization in the Arabidopsis embryo. Nature 353, 402–407
OpenUrl CrossRef

[94] Mayer U.,

[95] Torres Ruiz R. A.,

[96] Berleth T.,

[97] Misera S.,

[98] Jurgens G.

[99] Modrusan Z.,
Reiser L.,
Feldmann K. A.,
Fischer R. L.,
Haughn G. W.
(1994) Homeotic transformation of ovules into carpel-like structures in Arabidopsis. Plant Cell 6, 333–349
OpenUrl Abstract/FREE Full Text

[100] Modrusan Z.,

[101] Reiser L.,

[102] Feldmann K. A.,

[103] Fischer R. L.,

[104] Haughn G. W.

[105] Ray A.,
Robinson-Beers K.,
Ray S.,
Baker S. C.,
Lang J. D.,
Preuss D.,
Milligan S. B.,
Gasser C. S.
(1994) Arabidopsis floral homeotic gene BELL (BEL1) controls ovule development through negative regulation of AGAMOUS gene (AG). Proc. Natl. Acad. Sci. USA 91, 5761–5765
OpenUrl Abstract/FREE Full Text

[106] Ray A.,

[107] Robinson-Beers K.,

[108] Ray S.,

[109] Baker S. C.,

[110] Lang J. D.,

[111] Preuss D.,

[112] Milligan S. B.,

[113] Gasser C. S.

[114] Reiser L.,
Fischer R. L.
(1993) The ovule and the embryo sac. Plant Cell 5, 1291–1301
OpenUrl FREE Full Text

[115] Reiser L.,

[116] Fischer R. L.

[117] Reiser L.,
Modrusan Z. L. M.,
Samach A.,
Ohad N.,
Haughn G. W.,
Fischer R. L.
(1995) The BELL1 gene encodes a homeodomain protein involved in pattern formation in the Arabidopsis ovule primordium. Cell 83, 735–742
OpenUrl CrossRef PubMed Web of Science

[118] Reiser L.,

[119] Modrusan Z. L. M.,

[120] Samach A.,

[121] Ohad N.,

[122] Haughn G. W.,

[123] Fischer R. L.

[124] Robinson-Beers K.,
Pruitt R. E.,
Gasser C. S.
(1992) Ovule development in wild-type Arabidopsis and two female-sterile mutants. Plant Cell 4, 1237–1249
OpenUrl Abstract/FREE Full Text

[125] Robinson-Beers K.,

[126] Pruitt R. E.,

[127] Gasser C. S.

[128] Rounsley S. D.,
Ditta G. S.,
Yanofsky M. F.
(1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7, 1259–1269
OpenUrl Abstract/FREE Full Text

[129] Rounsley S. D.,

[130] Ditta G. S.,

[131] Yanofsky M. F.

[132] Sakai H.,
Medrano L. J.,
Meyerowitz E. M.
(1995) Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378, 199–203
OpenUrl CrossRef PubMed Web of Science

[133] Sakai H.,

[134] Medrano L. J.,

[135] Meyerowitz E. M.

[136] Savidge B.,
Rounsley S. D.,
Yanofsky M.
(1995) Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 7, 721–733
OpenUrl Abstract/FREE Full Text

[137] Savidge B.,

[138] Rounsley S. D.,

[139] Yanofsky M.

[140] Schneitz K.,
Hulskamp M.,
Pruitt R. E.
(1995) Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J 7, 731–749
OpenUrl CrossRef Web of Science

[141] Schneitz K.,

[142] Hulskamp M.,

[143] Pruitt R. E.

[144] Weigel D.
(1995) The APETALA2 domain is related to a novel type of DNA binding domain. Plant Cell 7, 388–389
OpenUrl FREE Full Text

[145] Weigel D.

[146] Weigel D.,
Meyerowitz E. M.
(1994) The abcs of floral homeotic genes. Cell 78, 203–209
OpenUrl CrossRef PubMed Web of Science

[147] Weigel D.,

[148] Meyerowitz E. M.

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The people behind the papers – George Britton and Aryeh Warmflash

Travelling Fellowship – New imaging approach unveils a bigger picture

Primer – Principles and applications of optogenetics in developmental biology

preLights – Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Spotlight – Can laboratory model systems instruct human limb regeneration?

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