Abstract
Although the hormonal control of root growth and development has been extensively studied, relatively little is known about the role that ethylene plays in cereal root development. In this work, we have investigated how the ethylene biosynthetic machinery is spatially regulated in maize roots and how changes in its expression alter root growth. ACC synthase (ZmACS) expression was observed in the root cap and in cortical cells whereas ACC oxidase (ZmACO) expression was detected in the root cap, protophloem sieve elements, and the companion cells associated with metaphloem sieve elements. Roots from Zmacs6 mutants exhibited significantly reduced ethylene production, a smaller root cap of increased cell number but smaller cell size, accelerated elongation of metaxylem, cortical, and epidermal cells, and increased vacuolation of cells in the calyptrogen of the root cap, phenotypes that were complemented by exogenous ACC. Zmacs6 mutant roots exhibited increased growth when largely unimpeded, a phenotype complemented by exogenous ACC, whereas loss of ZmACS2 expression had less of an effect. In contrast, Zmacs6 plants exhibited reduced root growth in soil. These results suggest that expression of ZmACS6 is important in regulating growth of maize roots in response to physical resistance.
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Abbreviations
- ACC:
-
1-Aminocyclopropane-1-carboxylic acid
- ACS:
-
ACC synthase
- ACO:
-
ACC oxidase
- AVG:
-
Aminoethoxyvinylglycine
- CC:
-
Companion cells
- eIF:
-
Eukaryotic initiation factor
- EtOH:
-
Ethanol
- MSE:
-
Metaphloem sieve element
- MS:
-
Murashige and Skoog
- QC:
-
Quiescent center
- qRT-PCR:
-
Quantitative RT-PCR
- (TIR)-PCR:
-
Terminal-inverted-repeat
- PSE:
-
Protophloem sieve element
- TE:
-
Tris–EDTA
- ZmXET :
-
Maize xyloglucan endo-transglycosylase
References
Abeles FB, Morgan PW, Saltveit ME Jr (1992) Ethylene in plant biology, 2nd edn. Academic Press Inc, San Diego, 414 pp
Amrhein N, Breuing F, Eberle J, Skorupka H, Tophof S (1982) The metabolism of l-aminocycloproprane-l-carboxylic acid. In: Waering PF (ed) Plant growth substances. Academic Press, New York, pp 249–258
Apelbaum A, Burg SP (1972) Effect of ethylene on cell division and deoxyribonucleic acid synthesis in Pisum sativum. Plant Physiol 50:117–124
Bensen RJ, Johal GS, Crane VC, Tossberg JT, Schnable PS, Meeley RB et al (1995) Cloning and characterization of the maize An1 gene. Plant Cell 7:75–84
Bradford KJ, Yang SF (1980) Xylem transport of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor, in waterlogged tomato plants. Plant Physiol 65:322–326
Buer CS, Wasteneys GO, Masle J (2003) Ethylene modulates root-wave responses in Arabidopsis. Plant Physiol 132:1085–1096. doi:10.1104/pp.102.019182
Buer CS, Sukumar P, Muday GK (2006) Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiol 140:1384–1396. doi:10.1104/pp.105.075671
Chang SC, Kim YS, Lee JY, Kaufman PB, Kirakosyan A, Yun HS et al (2004) Brassinolide interacts with auxin and ethylene in the root gravitropic response of maize (Zea mays). Physiol Plant 121:666–673. doi:10.1111/j.0031-9317.2004.00356.x
Clark DG, Gubrium EK, Barrett JE, Nell TA, Klee HJ (1999) Root formation in ethylene-insensitive plants. Plant Physiol 121:53–60. doi:10.1104/pp.121.1.53
Dolan L (1998) Pointing roots in the right direction: the role of auxin transport in response to gravity. Genes Dev 12:2091–2095. doi:10.1101/gad.12.14.2091
Ecker JR, Davis RW (1987) Plant defense genes are regulated by ethylene. Proc Natl Acad Sci USA 84:5202–5206. doi:10.1073/pnas.84.15.5202
Eleftheriou EP (1995) Phloem structure and cytochemistry. BIOS Thessaloniki 3:81–124
Feldman LJ (1984) Regulation of root development. Annu Rev Plant Physiol 35:223–242. doi:10.1146/annurev.pp.35.060184.001255
Finlayson SA, Foster KR, Reid DM (1991) Transport and metabolism of 1-aminocyclopropane-1-carboxylic acid in sunflower (Helianthus annuus L.) seedlings. Plant Physiol 96:1360–1367
Gallie DR, Young TE (2004) The ethylene biosynthetic and perception machinery is differentially expressed during endosperm and embryo development in maize. Mol Genet Genomics 271:267–281. doi:10.1007/s00438-004-0977-9
Grbic V, Bleecker AB (1995) Ethylene regulates the timing of leaf senescence in Arabidopsis. Plant J 8:595–602. doi:10.1046/j.1365-313X.1995.8040595.x
Jackson D (1991) In situ hybridization in plants. In: Bowles DJ, Gurr SJ, McPherson M (eds) Molecular plant pathology: a practical approach, vol 1. IRC Press, Oxford, pp 163–174
Jackson M (1997) Hormones from roots as signals for the shoots of stressed plants. Trends Plant Sci 2:22–28. doi:10.1016/S1360-1385(96)10050-9
John I, Drake R, Farrell A, Cooper W, Lee P, Horton P et al (1995) Delayed leaf senescence in ethylene-deficient ACC-oxidase antisense tomato plants: molecular and physiological analysis. Plant J 7:483–490. doi:10.1046/j.1365-313X.1995.7030483.x
Langdale JA (1994) In situ hybridization. In: Freeling M, Walbot V (eds) The maize handbook. Springer-Verlag, New York, pp 165–180
Le J, Vandenbussche F, Van Der Straeten D, Verbelen JP (2001) In the early response of Arabidopsis roots to ethylene, cell elongation is up- and down-regulated and uncoupled from differentiation. Plant Physiol 125:519–522. doi:10.1104/pp.125.2.519
Lee JS, Chang W-K, Evans ML (1990) Effects of ethylene on the kinetics of curvature and auxin redistribution in gravistimulated roots of Zea mays. Plant Physiol 94:1770–1775
Liang X, Abel S, Keller JA, Shen NF, Theologis A (1992) The 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana. Proc Natl Acad Sci USA 89:11046–11050. doi:10.1073/pnas.89.22.11046
Mattoo AK, Suttle JC (1991) The plant hormone ethylene. CRC Press, Boca Raton, 337 pp
Morgan P, Gausman H (1966) Effects of ethylene on auxin transport. Plant Physiol 41:45–52
Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, Kubo Y et al (1998) Differential expression and internal feedback regulation of 1-amino cyclopropane-1-carboxylate synthase, of 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol 118:1295–1305. doi:10.1104/pp.118.4.1295
Oparka KJ, Turgeon R (1999) Sieve elements and companion cells-traffic control centers of the phloem. Plant Cell 11:739–750
Ortega-Martínez O, Pernas M, Carol RJ, Dolan L (2007) Ethylene modulates stem cell division in the Arabidopsis thaliana root. Science 317:507–510. doi:10.1126/science.1143409
Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560. doi:10.1046/j.1365-313x.1998.00321.x
Ponce G, Barlow PW, Feldman LJ, Cassab GI (2005) Auxin and ethylene interactions control mitotic activity of the quiescent centre, root cap size, and pattern of cap cell differentiation in maize. Plant Cell Environ 28:719–732. doi:10.1111/j.1365-3040.2005.01318.x
Ruzicka K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Friml J et al (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212. doi:10.1105/tpc.107.052126
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning—a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Sarquis JI, Jordan WR, Morgan PW (1991) Ethylene evolution from maize (Zea mays L.) seedling roots and shoots in response to mechanical impedance. Plant Physiol 96:1171–1177
Schiefelbein JW (2000) Constructing a plant cell. The genetic control of root hair development. Plant Physiol 124:1525–1531. doi:10.1104/pp.124.4.1525
Sell S, Hehl R (2005) A fifth member of the tomato 1-aminocyclopropane-1-carboxylic acid (ACC) oxidase gene family harbours a leucine zipper and is anaerobically induced. DNA Seq 16:80–82. doi:10.1080/10425170500050817
Sjolund RD (1997) The phloem sieve element: a river runs through it. Plant Cell 9:1137–1146. doi:10.1105/tpc.9.7.1137
Smalle J, Haegman M, Kurepa J, Van Montagu M, Straeten DV (1997) Ethylene can stimulate Arabidopsis hypocotyl elongation in the light. Proc Natl Acad Sci USA 94:2756–2761. doi:10.1073/pnas.94.6.2756
Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM (2005) A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17:2230–2242. doi:10.1105/tpc.105.033365
Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19:2169–2185. doi:10.1105/tpc.107.052068
Suttle JC (1988) Effect of ethylene treatment on polar IAA transport, net IAA uptake and specific binding of N-1-naphthylphthalamic acid in tissues and microsomes isolated from etiolated pea epicotyls. Plant Physiol 88:795–799
Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GT, Sandberg G et al (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196. doi:10.1105/tpc.107.052100
Tsuchisaka A, Theologis A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol 136:2982–3000. doi:10.1104/pp.104.049999
Tudela D, Primo-Millo E (1992) 1-Aminocyclopropane-1-carboxylic acid transported from roots to shoots promotes leaf abscission in Cleopatra Mandarin (Citrus reshni Hort. ex Tan.) seedlings rehydrated after water stress. Plant Physiol 100:131–137
Van Der Straeten D, Zhou Z, Prinsen E, Van Onckelen HA, Van Montagu MC (2001) A comparative molecular-physiological study of submergence response in lowland and deepwater rice. Plant Physiol 125:955–968. doi:10.1104/pp.125.2.955
Whalen MC, Feldman LJ (1988) The effect of ethylene on root growth of Zea mays seedlings. Can J Bot 66:719–723
Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189. doi:10.1146/annurev.pp.35.060184.001103
Young TE, Gallie DR, DeMason DA (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Physiol 115:737–751
Young TE, Meeley RB, Gallie DR (2004) ACC synthase expression regulates leaf performance and drought tolerance in maize. Plant J 40:813–825. doi:10.1111/j.1365-313X.2004.02255.x
Zacarias L, Reid MS (1992) Inhibition of ethylene action prevents root penetration through compressed media in tomato (Lycopersicon esculentum) seedlings. Physiol Plant 86:301–307. doi:10.1034/j.1399-3054.1992.860217.x
Zarembinski TI, Theologis A (1994) Ethylene biosynthesis and action: a case of conservation. Plant Mol Biol 26:1579–1597. doi:10.1007/BF00016491
Zhou Z, Vriezen W, Caeneghem W, Van Montagu M, Van Der Straeten D (2001) Rapid induction of a novel ACC synthase gene in deepwater rice seedlings upon complete submergence. Euphytica 121:137–143. doi:10.1023/A:1012059425624
Zhou Z, de Almeida Engler J, Rouan D, Michiels F, Van Montagu M, Van Der Straeten D (2002) Tissue localization of a submergence-induced 1-aminocyclopropane-1-carboxylic acid synthase in rice. Plant Physiol 129:72–84. doi:10.1104/pp.001206
Acknowledgments
The authors thank Todd Young for the initial analysis of the mutant roots and Christian Caldwell for technical assistance. This work was supported by grant NRICGP 2002-35100-12469 from the United States Department of Agriculture and the University of California Agricultural Experiment Station.
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Gallie, D.R., Geisler-Lee, J., Chen, J. et al. Tissue-specific expression of the ethylene biosynthetic machinery regulates root growth in maize. Plant Mol Biol 69, 195–211 (2009). https://doi.org/10.1007/s11103-008-9418-1
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DOI: https://doi.org/10.1007/s11103-008-9418-1