Abstract
Increasing its root to shoot ratio is a plant strategy for restoring water homeostasis in response to the long-term imposition of mild water stress. In addition to its important role in diverse fundamental processes, indole-3-acetic acid (IAA) is involved in root growth and development. Recent extensive characterizations of the YUCCA gene family in Arabidopsis and rice have elucidated that member’s function in a tryptophan-dependent IAA biosynthetic pathway. Through forward- and reverse-genetics screening, we have isolated Tos17 and T-DNA insertional rice mutants in a CONSTITUTIVELY WILTED1 (COW1) gene, which encodes a new member of the YUCCA protein family. Homozygous plants with either a Tos17 or T-DNA-inserted allele of OsCOW1 exhibit phenotypes of rolled leaves, reduced leaf widths, and lower root to shoot ratios. These phenotypes are evident in seedlings as early as 7–10 d after germination, and remain until maturity. When oscow1 seedlings are grown under low-intensity light and high relative humidity, the rolled-leaf phenotype is greatly alleviated. For comparison, in such conditions, the transpiration rate for WT leaves decreases approx. 5- to 10-fold, implying that this mutant trait results from wilting rather than being a morphogenic defect. Furthermore, a lower turgor potential and transpiration rate in their mature leaves indicates that oscow1 plants are water-deficient, due to insufficient water uptake that possibly stems from that diminished root to shoot ratio. Thus, our observations suggest that OsCOW1-mediated IAA biosynthesis plays an important role in maintaining root to shoot ratios and, in turn, affects water homeostasis in rice.
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References
An G, Jeong D-H, Jung K-H, Lee S (2005) Reverse genetic approaches for functional genomics of rice. Plant Mol Biol 59:111–123
An S, Park S, Jeong D-H, Lee D-Y, Kang H-G, Yu J-H, Hur J, Kim S-R, Kim Y-H, Lee M, Han S, Kim S-J, Yang J, Kim E, Wi SJ, Chung HS, Hong J-P, Choe V, Lee H-K, Choi J-H, Nam J, Kim S-R, Park P-B, Park KY, Kim WT, Choe S, Lee C-B, An G (2003) Generation and analysis of end-sequence database for T-DNA tagging lines in rice. Plant Physiol 133:2040–2047
Bartel B (1997) Auxin biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 48:51–66
Champoux MC, Wang G, Sarkarung S, Mackill DJ, O’Toole JC, Huang N, McCouch SR (1995) Locating genes associated with root morphology and drought avoidance in rice via linkage to molecular markers. Theor Appl Genet 90:969–981
Chen Z, Hong X, Zhang H, Wang Y, Li X, Zhu J-K, Gong Z (2005) Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J 43:273–283
Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20:1790–1799
Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995
Cohen JD, Slovin JP, Hendrickson AM (2003) Two genetically discrete pathways convert tryptophan to auxin: More redundancy in auxin biosynthesis. Trends Plant Sci 8:197–199
Fukai S, Cooper M (1995) Development of drought-resistant cultivars using physio-morphological traits in rice. Field Crops Res 40:67–86
Han M-J, Jung K-H, Yi G, Lee D-Y, An G (2006) Rice Immature Pollen 1 (RIP1) is a regulator of late pollen development. Plant Cell Physiol 47:1457–1472
Hull AK, Vij R, Celenza JL (2000) Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis. Proc Natl Acad Sci USA 97:2379–2384
Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura I, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17:1387–1396
Ishihara K, Hirasawa T, Iida O, Kimura M (1981) Diurnal course of transpiration rate, stomatal aperture, stomatal conductance, xylem water potential and leaf water potential in the rice plants under the different growth conditions. Jpn J Crop Sci 50:25–37
Jang S-M, Ishihara A, Back K (2004) Production of coumaroylserotonin and feruloylserotonin in transgenic rice expressing pepper hydroxycinnamoyl-Coenzyme A: serotonin N-(hydroxycinnamoyl) transferase. Plant Physiol 135:346–356
Jeon J-S, Lee S, Jung K-H, Jun S-H, Jeong D-H, Lee J, Kim C, Jang S, Lee S-Y, Yang K, Nam J-M, An K, Han M-J, Sung R-J, Choi H-S, Yu J-W, Choi J-H, Cho S-Y, Cha S-S, An G (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22:561–570
Jeong DH, An S, Kang HG, Moon S, Han JJ, Park S, Lee HS, An K, An G (2002) T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiol 130:1636–1644
Jeong D-H, An S, Park S, Kang H-G, Park G-G, Kim S-R, Sim J, Kim Y-O, Kim M-K, Kim S-R, Kim J, Shin M, Jung M, An G (2006) Generation of flanking sequence-tag database for activation-tagging lines in japonica rice. Plant J 45:123–132
Jung KH, Hur J, Ryu CH, Choi Y, Chung YY, Miyao A, Hirochika H, An G (2003) Characterization of a rice chlorophyll-deficient mutant using the T-DNA gene-trap system. Plant Cell Physiol 44:463–472
Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G (2005) Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17:2705–2722
Li Z, Mu P, Li C, Zhang H, Li Z, Gao Y, Wang X (2005) QTL mapping of root traits in a doubled haploid population from a cross between upland and lowland japonica rice in three environments. Theor Appl Genet 110:1244–1252
Liu H, Wang S, Yu X, Yu J, He X, Zhang S, Shou H, Wu P (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J 43:47–56
Ljung K, Bhalerao RP, Sandberg G (2001) Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J 28:465–474
Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G (2002) Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol 49:249–272
Michalczuk L, Ribnicky DM, Cooke TJ, Cohen JD (1992) Regulation of indole-3-acetic acid biosynthetic pathways in carrot cell cultures. Plant Physiol 100:1346–1353
Mikkelsen MD, Hansen CH, Wittstock U, Halkier BA (2000) Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. J Biol Chem 275:33712–33717
Miyamoto N, Steudle E, Hirasawa T, Lafitte R (2001) Hydraulic conductivity of rice roots. J Exp Bot 52:1835–1846
Moon S, Jung KH, Lee DE, Lee DY, Lee J, An K, Kang HG, An G (2006) The rice FON1 gene controls vegetative and reproductive development by regulating shoot apical meristem size. Mol Cells 21:147–152
Müller A, Hillebrand H, Weiler EW (1998) Indole-3-acetic acid is synthesized from L-tryptophan in roots of Arabidopsis thaliana. Planta 206:362–369
Normanly J, Bartel B (1999) Redundancy as a way of life - IAA metabolism. Curr Opin Plant Biol 2:207–213
Normanly J, Cohen JD, Fink GR (1993) Arabidopsis thaliana auxotrophs reveal a tryptophan-independent biosynthetic pathway for indole-3-acetic acid. Proc Natl Acad Sci USA 90:10355–10359
Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: Developments in root system architecture. Annu Rev Plant Biology 58:93–113
Östin A, Ili´c N, Cohen JD (1999) An in vitro system for tryptophan-independent indole-3-acetic acid biosynthesis from Zea mays seedlings. Plant Physiol 119:173–178
Park M, Kim SJ, Vitale A, Hwang I (2004) Identification of the protein storage vacuole and protein targeting to the vacuole in leaf cells of three plant species. Plant Physiol 134:625–639
Price AH, Virk DS, Tomos AD (1997) Genetic dissection of root growth in rice (Oryza sativa L.). I: A hydroponic screen. Theor Appl Genet 95:132–142
Quirino B, Normanly J, Amasino R (1999) Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Mol Biol 40:267–278
Ryu C-H, You J-H, Kang H-G, Hur J, Kim Y-H, Han M-J, An K, Chung B-C, Lee C-H, An G (2004) Generation of T-DNA gene tagging lines with a bidirectional gene trap vector and the establishment of an insertion-site database. Plant Mol Biol 54:489–502
Schmidt RC, Müller A, Hain R, Bartling D, Weiler EW (1996) Transgenic tobacco plants expressing the Arabidopsis nitrilase II enzyme. Plant J 9:683–691
Schreiber L, Franke R, Hartmann K-D, Ranathunge K, Steudle E (2005) The chemical composition of suberin in apoplastic barriers affects radial hydraulic conductivity differently in the roots of rice (Oryza sativa L. cv. IR64) and corn (Zea mays L. cv. Helix). J Exp Bot 56:1427–1436
Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: Physiology to functional genomics. J Exp Bot 55:2343–2351
Sitbon F, Åstot C, Edlund A, Crozier A, Sandberg G (2000) The relative importance of tryptophan-dependent and tryptophan-independent biosynthesis of indole-3-acetic acid in tobacco during vegetative growth. Planta 211:715–721
Spertini D, Beliveau C, Bellemare G (1999) Screening of transgenic plants by amplification of unknown genomic DNA flanking T-DNA. Biotechniques 27:308–314
Tobeña-Santamaria R, Bliek M, Ljung K, Sandberg G, Mol JNM, Souer E, Koes R (2002) FLOOZY of petunia is a flavin mono-oxygenase-like protein required for the specification of leaf and flower architecture. Genes Dev 16:753–763
Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu J-K (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539
Woodward AW, Bartel B (2005) Auxin: Regulation, action, and interaction. Ann Bot 95:707–735
Woodward C, Bemis SM, Hill EJ, Sawa S, Koshiba T, Torii KU (2005) Interaction of auxin and ERECTA in elaborating Arabidopsis inflorescence architecture revealed by the activation tagging of a new member of the YUCCA family putative flavin monooxygenases. Plant Physiol 139:192–203
Wright AD, Sampson MB, Neuffer MG, Michalczuk L, Slovin JP, Cohen JD (1991) Indole-3-acetic acid biosynthesis in the mutant maize orange pericarp, a tryptophan auxotroph. Science 254:998–1000
Yamamoto Y, Kamiya N, Morinaka Y, Matsuoka M, Sazuka T (2007) Auxin biosynthesis by the YUCCA genes in rice. Plant Physiol 143:1362–1371
Ye Z-H (2002) Vascular tissue differentiation and pattern formation in plants. Annu Rev Plant Biol 53:183–202
Zhang J, Nguyen H, Blum A (1999) Genetic analysis of osmotic adjustment in crop plants. J Exp Bot 50:291–302
Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306–309
Zhao Y, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J, Celenza JL (2002) (Trp)-dependent auxin biosynthesis in Arabidopsis: Involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16:3100–3112
Acknowledgements
We thank In-Soon Park and Kyungsook An for generating the T-DNA insertional lines, Yoonja Cho for managing the transgenic seeds, Chang-Duk Jung for growing the transformed plants, and Priscilla Licht for English editing of the manuscript. This work was supported, in part, by grants from the Crop Functional Genomic Center, the 21st Century Frontier Program (Grant CG1111); from the Biogreen 21 Program, Rural Development Administration; and from the Korea Science and Engineering Foundation (KOSEF) through the National Research Laboratory Program funded by the Ministry of Science and Technology (M10600000270-06J0000-27010).
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Woo, YM., Park, HJ., Su’udi, M. et al. Constitutively wilted 1, a member of the rice YUCCA gene family, is required for maintaining water homeostasis and an appropriate root to shoot ratio. Plant Mol Biol 65, 125–136 (2007). https://doi.org/10.1007/s11103-007-9203-6
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DOI: https://doi.org/10.1007/s11103-007-9203-6