Divide et impera: Boundaries shape the plant body and initiate new meristems

New Phytologist

Volumn 209, Issue 2, 2016, Pages 485-498

  Wang, Quan ^a   Hasson, Alice ^a   Rossmann, Susanne ^a   Theres, Klaus ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

Arabidopsis; Axillary meristem; Boundary zone; Compound leaf; Ectopic meristem; Tomato (Solanum lycopersicum)

Indexed keywords

BODY SHAPE; CELLS AND CELL COMPONENTS; DICOTYLEDON; FRUIT; GENE EXPRESSION; HORMONE; LEAF; STEROID;

ARABIDOPSIS; LYCOPERSICON ESCULENTUM;

BRASSINOSTEROID; INDOLEACETIC ACID DERIVATIVE;

CELL DIVISION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM; PLANT LEAF; SHOOT;

BRASSINOSTEROIDS; CELL DIVISION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INDOLEACETIC ACIDS; MERISTEM; PLANT LEAVES; PLANT SHOOTS;

EID: 84955183255     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13641     Document Type: Review

References (98)

1. Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M. 1997. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9: 841-857.
2. Aida M, Ishida T, Tasaka M. 1999. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126: 1563-1570.
3. Barkoulas M, Hay A, Kougioumoutzi E, Tsiantis M. 2008. A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nature Genetics 40: 1136-1141.
4. Barton MK. 2010. Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Developmental Biology 341: 95-113.
5. Barton MK, Poethig RS. 1993. Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild type and in the shoot meristemless mutant. Development 119: 823-831.
6. Bayer EM, Smith RS, Mandel T, Nakayama N, Sauer M, Prusinkiewicz P, Kuhlemeier C. 2009. Integration of transport-based models for phyllotaxis and midvein formation. Genes & Development 23: 373-384.
7. Bell EM, Lin WC, Husbands AY, Yu L, Jaganatha V, Jablonska B, Mangeon A, Neff MM, Girke T, Springer PS. 2012. Arabidopsis LATERAL ORGAN BOUNDARIES negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proceedings of the National Academy of Sciences, USA 109: 21146-21151.
8. Ben-Gera H, Shwartz I, Shao M-R, Shani E, Estelle M, Ori N. 2012. ENTIRE and GOBLET promote leaflet development in tomato by modulating auxin response. Plant Journal 70: 903-915.
9. Berger Y, Harpaz-Saad S, Brand A, Melnik H, Sirding N, Alvarez JP, Zinder M, Samach A, Eshed Y, Ori N. 2009. The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136: 823-832.
10. Bilsborough GD, Runions A, Barkoulas M, Jenkins HW, Hasson A, Galinha C, Laufs P, Hay A, Prusinkiewicz P, Tsiantis M. 2011. Model for the regulation of Arabidopsis thaliana leaf margin development. Proceedings of the National Academy of Sciences, USA 108: 3424-3429.
11. Blein T, Pulido A, Vialette-Guiraud A, Nikovics K, Morin H, Hay A, Johansen IE, Tsiantis M, Laufs P. 2008. A conserved molecular framework for compound leaf development. Science 322: 1835-1839.
12. Borghi L, Bureau M, Simon R. 2007. Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity. Plant Cell 19: 1795-1808.
13. Bortiri E, Chuck G, Vollbrecht E, Rocheford T, Martienssen R, Hake S. 2006. ramosa2 encodes a LATERAL ORGAN BOUNDARY domain protein that determines the fate of stem cells in branch meristems of maize. Plant Cell 18: 574-585.
14. Brand A, Shirding N, Shleizer S, Ori N. 2007. Meristem maintenance and compound-leaf patterning utilize common genetic mechanisms in tomato. Planta 226: 941-951.
15. Breuil-Broyer S, Morel P, De Almeida-Engler J, Coustham V, Negrutiu I, Trehin C. 2004. High-resolution boundary analysis during Arabidopsis thaliana flower development. Plant Journal 38: 182-192.
16. Bureau M, Rast M, Illmer J, Simon R. 2010. JAGGED LATERAL ORGAN (JLO) controls auxin dependent patterning during development of the Arabidopsis embryo and root. Plant Molecular Biology 74: 479-491.
17. Busch BL, Schmitz G, Rossmann S, Piron F, Ding J, Bendahmane A, Theres K. 2011. Shoot branching and leaf dissection in tomato are regulated by homologous gene modules. Plant Cell 23: 3595-3609.
18. Chen J, Moreau C, Liu Y, Kawaguchi M, Hofer J, Ellis N, Chen R. 2012. Conserved genetic determinant of motor organ identity in Medicago truncatula and related legumes. Proceedings of the National Academy of Sciences, USA 109: 11723-11728.
19. Cheng X, Peng J, Ma J, Tang Y, Chen R, Mysore KS, Wen J. 2012. NO APICAL MERISTEM (MtNAM) regulates floral organ identity and lateral organ separation in Medicago truncatula. New Phytologist 195: 71-84.
20. Cheng Y, Dai X, Zhao Y. 2007. Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19: 2430-2439.
21. Cho E, Zambryski PC. 2011. ORGAN BOUNDARY1 defines a gene expressed at the junction between the shoot apical meristem and lateral organs. Proceedings of the National Academy of Sciences, USA 108: 2154-2159.
22. Chuck G, Whipple C, Jackson D, Hake S. 2010. The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries. Development 137: 1243-1250.
23. Couzigou J-M, Zhukov V, Mondy S, Abu el Heba G, Cosson V, Ellis THN, Ambrose M, Wen J, Tadege M, Tikhonovich I et al. 2012. NODULE ROOT and COCHLEATA maintain nodule development and are legume orthologs of Arabidopsis BLADE-ON-PETIOLE genes. Plant Cell 24: 4498-4510.
24. Dharmasiri N, Dharmasiri S, Estelle M. 2005. The F-box protein TIR1 is an auxin receptor. Nature 435: 441-445.
25. Eviatar-Ribak T, Shalit-Kaneh A, Chappell-Maor L, Amsellem Z, Eshed Y, Lifschitz E. 2013. A cytokinin-activating enzyme promotes tuber formation in tomato. Current Biology 23: 1057-1064.
26. Floyd S, Bowman J. 2010. Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology? Journal of Plant Research 123: 43-55.
27. Furutani M, Vernoux T, Traas J, Kato T, Tasaka M, Aida M. 2004. PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis. Development 131: 5021-5030.
28. Gallavotti A, Barazesh S, Malcomber S, Hall D, Jackson D, Schmidt RJ, McSteen P. 2008a. sparse inflorescence1 encodes a monocot-specific YUCCA-like gene required for vegetative and reproductive development in maize. Proceedings of the National Academy of Sciences, USA 105: 15196-15201.
29. Gallavotti A, Yang Y, Schmidt RJ, Jackson D. 2008b. The relationship between auxin transport and maize branching. Plant Physiology 147: 1913-1923.
30. Gallavotti A, Zhao Q, Kyozuka J, Meeley RB, Ritter MK, Doebley JF, Enrico Pe M, Schmidt RJ. 2004. The role of barren stalk1 in the architecture of maize. Nature 432: 630-635.
31. Gendron JM, Liu J-S, Fan M, Bai M-Y, Wenkel S, Springer PS, Barton MK, Wang Z-Y. 2012. Brassinosteroids regulate organ boundary formation in the shoot apical meristem of Arabidopsis. Proceedings of the National Academy of Sciences, USA 109: 21152-21157.
32. Greb T, Clarenz O, Schäfer E, Müller D, Herrero R, Schmitz G, Theres K. 2003. Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes & Development 17: 1175-1187.
33. Ha CM, Jun JH, Nam HG, Fletcher JC. 2004. BLADE-ON-PETIOLE1 encodes a BTB/POZ domain protein required for leaf morphogenesis in Arabidopsis thaliana. Plant and Cell Physiology 45: 1361-1370.
34. Ha CM, Jun JH, Nam HG, Fletcher JC. 2007. BLADE-ON-PETIOLE1 and 2 control Arabidopsis lateral organ fate through regulation of LOB domain and adaxial-abaxial polarity genes. Plant Cell 19: 1809-1825.
35. Ha CM, Kim G-T, Kim BC, Jun JH, Soh MS, Ueno Y, Machida Y, Tsukaya H, Nam HG. 2003. The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development 130: 161-172.
36. Hagemann W, Gleissberg S. 1996. Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms. Plant Systematics and Evolution 199: 121-152.
37. Hamant O, Heisler MG, Jönsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM et al. 2008. Developmental patterning by mechanical signals in Arabidopsis. Science 322: 1650-1655.
38. Han Y, Zhang C, Yang H, Jiao Y. 2014. Cytokinin pathway mediates APETALA1 function in the establishment of determinate floral meristems in Arabidopsis. Proceedings of the National Academy of Sciences, USA 111: 6840-6845.
39. Heisler MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C, Jönsson H, Traas J, Meyerowitz EM. 2010. Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biology 8: e1000516.
40. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM. 2005. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Current Biology 15: 1899-1911.
41. Hepworth SR, Zhang Y, McKim S, Li X, Haughn GW. 2005. BLADE-ON-PETIOLE-dependent signaling controls leaf and floral patterning in Arabidopsis. Plant Cell 17: 1434-1448.
42. Hibara K, Karim MR, Takada S, Taoka K, Furutani M, Aida M, Tasaka M. 2006. Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell 18: 2946-2957.
43. Hussey G. 1971. In vitro growth of vegetative tomato shoot apices. Journal of Experimental Botany 22: 688-701.
44. Jeifetz D, David-Schwartz R, Borovsky Y, Paran I. 2011. CaBLIND regulates axillary meristem initiation and transition to flowering in pepper. Planta 234: 1227-1236.
45. Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X et al. 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nature Genetics 42: 541-544.
46. Kawamura E, Horiguchi G, Tsukaya H. 2010. Mechanisms of leaf tooth formation in Arabidopsis. Plant Journal 62: 429-441.
47. Keller T, Abbott J, Moritz T, Doerner P. 2006. Arabidopsis REGULATOR OF AXILLARY MERISTEMS1 controls a leaf axil stem cell niche and modulates vegetative development. Plant Cell 18: 598-611.
48. Kepinski S, Leyser O. 2005. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435: 446-451.
49. Khan M, Xu H, Hepworth SR. 2014. BLADE-ON-PETIOLE genes: setting boundaries in development and defense. Plant Science 215-216: 157-171.
50. Koenig D, Bayer E, Kang J, Kuhlemeier C, Sinha N. 2009. Auxin patterns Solanum lycopersicum leaf morphogenesis. Development 136: 2997-3006.
51. Komatsu K, Maekawa M, Ujiie S, Satake Y, Furutani I, Okamoto H, Shimamoto K, Kyozuka J. 2003. LAX and SPA: major regulators of shoot branching in rice. Proceedings of the National Academy of Sciences, USA 100: 11765-11770.
52. Kwiatkowska D, Dumais J. 2003. Growth and morphogenesis at the vegetative shoot apex of Anagallis arvensis L. Journal of Experimental Botany 54: 1585-1595.
53. Laufs P, Peaucelle A, Morin H, Traas J. 2004. MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 131: 4311-4322.
54. Lee D-K, Geisler M, Springer PS. 2009. LATERAL ORGAN FUSION1 and LATERAL ORGAN FUSION2 function in lateral organ separation and axillary meristem formation in Arabidopsis. Development 136: 2423-2432.
55. Leyser O. 2006. Dynamic integration of auxin transport and signalling. Current Biology 16: R424-R433.
56. Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F et al. 2003. Control of tillering in rice. Nature 422: 618-621.
57. Liscum E, Reed JW. 2002. Genetics of Aux/IAA and ARF action in plant growth and development. In: Perrot-Rechenmann C, Hagen G, eds. Auxin molecular biology: Dordrecht, the Netherlands: Springer, 387-400.
58. Mapelli S, Kinet JM. 1992. Plant growth regulator and graft control of axillary bud formation and development in the TO-2 mutant tomato. Plant Growth Regulators 11: 385-390.
59. McSteen P, Hake S. 2001. barren inflorescence2 regulates axillary meristem development in the maize inflorescence. Development 128: 2881-2891.
60. McSteen P, Malcomber S, Skirpan A, Lunde C, Wu X, Kellogg E, Hake S. 2007. barren inflorescence2 encodes a co-ortholog of the PINOID serine/threonine kinase and is required for organogenesis during inflorescence and vegetative development in maize. Plant Physiology 144: 1000-1011.
61. Miura K, Ikeda M, Matsubara A, Song X-J, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M. 2010. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nature Genetics 42: 545-549.
62. Müller D, Schmitz G, Theres K. 2006. Blind homologous R2R3 Myb genes control the pattern of lateral meristem initiation in Arabidopsis. Plant Cell 18: 586-597.
63. Müller D, Waldie T, Miyawaki K, To JPC, Melnyk CW, Kieber JJ, Kakimoto T, Leyser O. 2015. Cytokinin is required for escape but not release from auxin mediated apical dominance. Plant Journal 82: 874-886.
64. Naz AA, Raman S, Martinez CC, Sinha NR, Schmitz G, Theres K. 2013. Trifoliate encodes an MYB transcription factor that modulates leaf and shoot architecture in tomato. Proceedings of the National Academy of Sciences, USA 110: 2401-2406.
65. Norberg M, Holmlund M, Nilsson O. 2005. The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development 132: 2203-2213.
66. Oikawa T, Kyozuka J. 2009. Two-Step regulation of LAX PANICLE1 protein accumulation in axillary meristem formation in rice. Plant Cell 21: 1095-1108.
67. Phillips KA, Skirpan AL, Liu X, Christensen A, Slewinski TL, Hudson C, Barazesh S, Cohen JD, Malcomber S, McSteen P. 2011. vanishing tassel2 encodes a grass-specific tryptophan aminotransferase required for vegetative and reproductive development in maize. Plant Cell 23: 550-566.
68. Raman S, Greb T, Peaucelle A, Blein T, Laufs P, Theres K. 2008. Interplay of miR164, CUP-SHAPED COTYLEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. Plant Journal 55: 65-76.
69. Rast MI, Simon R. 2012. Arabidopsis JAGGED LATERAL ORGANS acts with ASYMMETRIC LEAVES2 to coordinate KNOX and PIN expression in shoot and root meristems. Plant Cell 24: 2917-2933.
70. Reddy GV, Heisler MG, Ehrhardt DW, Meyerowitz EM. 2004. Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development 131: 4225-4237.
71. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C. 2003. Regulation of phyllotaxis by polar auxin transport. Nature 426: 255-260.
72. Ritter MK, Padilla CM, Schmidt RJ. 2002. The maize mutant barren stalk1 is defective in axillary meristem development. American Journal of Botany 89: 203-210.
73. Rossmann S, Kohlen W, Hasson A, Theres K. 2015. Lateral suppressor and Goblet act in hierarchical order to regulate ectopic meristem formation at the base of tomato leaflets. Plant Journal 81: 837-848.
74. Schmitz G, Tillmann E, Carriero F, Fiore C, Cellini F, Theres K. 2002. The tomato Blind gene encodes a MYB transcription factor that controls the formation of lateral meristems. Proceedings of the National Academy of Sciences, USA 99: 1064-1069.
75. Schumacher K, Schmitt T, Rossberg M, Schmitz G, Theres K. 1999. The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proceedings of the National Academy of Sciences, USA 96: 290-295.
76. Shani E, Ben-Gera H, Shleizer-Burko S, Burko Y, Weiss D, Ori N. 2010. Cytokinin regulates compound leaf development in tomato. Plant Cell 22: 3206-3217.
77. Shuai B, Reynaga-Peña CG, Springer PS. 2002. The LATERAL ORGAN BOUNDARIES gene defines a novel, plant-specific gene family. Plant Physiology 129: 747-761.
78. Sicard A, Thamm A, Marona C, Lee Young W, Wahl V, Stinchcombe JR, Wright SI, Kappel C, Lenhard M. 2014. Repeated evolutionary changes of leaf morphology caused by mutations to a homeobox gene. Current Biology 24: 1880-1886.
79. Skirpan A, Culler AH, Gallavotti A, Jackson D, Cohen JD, McSteen P. 2009. BARREN INFLORESCENCE2 interaction with ZmPIN1a suggests a role in auxin transport during maize inflorescence development. Plant and Cell Physiology 50: 652-657.
80. Sorefan K, Girin T, Liljegren SJ, Ljung K, Robles P, Galvan-Ampudia CS, Offringa R, Friml J, Yanofsky MF, Ostergaard L. 2009. A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 459: 583-586.
81. Souer E, van Houwelingen A, Kloos D, Mol J, Koes R. 1996. The No Apical Meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 85: 159-170.
82. Takada S, Hibara K, Ishida T, Tasaka M. 2001. The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128: 1127-1135.
83. Takeda S, Hanano K, Kariya A, Shimizu S, Zhao L, Matsui M, Tasaka M, Aida M. 2011. CUP-SHAPED COTYLEDON1 transcription factor activates the expression of LSH4 and LSH3, two members of the ALOG gene family, in shoot organ boundary cells. Plant Journal 66: 1066-1077.
84. Tantikanjana T, Yong JWH, Letham DS, Griffith M, Hussain M, Ljung K, Sandberg G, Sundaresan V. 2001. Control of axillary bud initiation and shoot architecture in Arabidopsis through the SUPERSHOOT gene. Genes & Development 15: 1577-1588.
85. Tavakol E, Okagaki R, Verderio G, Shariati V, Hussien A, Bilgic H, Scanlon MJ, Todt NR, Close TJ, Druka A et al. 2015. The barley Uniculme4 gene encodes a BLADE-ON-PETIOLE-like protein that controls tillering and leaf patterning. Plant Physiology 168: 164-174.
86. Tian C, Zhang X, He J, Yu H, Wang Y, Shi B, Han Y, Wang G, Feng X, Zhang C et al. 2014. An organ boundary-enriched gene regulatory network uncovers regulatory hierarchies underlying axillary meristem initiation. Molecular Systems Biology 10: 755.
87. Vernoux T, Brunoud G, Farcot E, Morin V, Van den Daele H, Legrand J, Oliva M, Das P, Larrieu A, Wells D et al. 2011. The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Molecular Systems Biology 7: 508.
88. Vlad D, Kierzkowski D, Rast MI, Vuolo F, Dello Ioio R, Galinha C, Gan X, Hajheidari M, Hay A, Smith RS et al. 2014. Leaf shape evolution through duplication, regulatory diversification, and loss of a homeobox gene. Science 343: 780-783.
89. Vroemen CW, Mordhorst AP, Albrecht C, Kwaaitaal MACJ, de Vries SC. 2003. The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15: 1563-1577.
90. Wang Q, Kohlen W, Rossmann S, Vernoux T, Theres K. 2014a. Auxin depletion from the leaf axil conditions competence for axillary meristem formation in Arabidopsis and tomato. Plant Cell 26: 2068-2079.
91. Wang Y, Wang J, Shi B, Yu T, Qi J, Meyerowitz EM, Jiao Y. 2014b. The stem cell niche in leaf axils is established by auxin and cytokinin in Arabidopsis. Plant Cell 26: 2055-2067.
92. Wardlaw C. 1943. Experimental and analytical studies of Pteridophytes I. Preliminary observations on the development of buds on the rhizome of the ostrich fern (Matteuccia struthiopteris Tod.). Annals of Botany 7: 171-184.
93. Weir I, Lu J, Cook H, Causier B, Schwarz-Sommer Z, Davies B. 2004. CUPULIFORMIS establishes lateral organ boundaries in Antirrhinum. Development 131: 915-922.
94. Wu X, McSteen P. 2007. The role of auxin transport during inflorescence development in maize (Zea mays, Poaceae). American Journal of Botany 94: 1745-1755.
95. Yang F, Wang Q, Schmitz G, Müller D, Theres K. 2012. The bHLH protein ROX acts in concert with RAX1 and LAS to modulate axillary meristem formation in Arabidopsis. Plant Journal 71: 61-70.
96. Yoshida A, Suzaki T, Tanaka W, Hirano H-Y. 2009. The homeotic gene long sterile lemma (G1) specifies sterile lemma identity in the rice spikelet. Proceedings of the National Academy of Sciences, USA 106: 20103-20108.
97. Zhao H, Liu L, Mo H, Qian L, Cao Y, Cui S, Li X, Ma L. 2013. The ATP-binding cassette transporter ABCB19 regulates postembryonic organ separation in Arabidopsis. PLoS ONE 8: e60809.
98. Zhou C, Han L, Fu C, Chai M, Zhang W, Li G, Tang Y, Wang Z-Y. 2012. Identification and characterization of petiolule-like pulvinus mutants with abolished nyctinastic leaf movement in the model legume Medicago truncatula. New Phytologist 196: 92-100.