Abstract
Main conclusion
Morphological and genetic markers indicate that in sorghum, the juvenile-to-adult phase transition occurs during the fourth and fifth leaf stages. This timing differs from those reported for other plants.
Abstract
The juvenile-to-adult (JA) phase transition is an important event for optimizing vegetative growth and reproductive success in plants. Among the Poaceae crops, which are a vital food source for humans, studies of the JA phase transition have been restricted to rice and maize. We studied the morphological and genetic changes that occur during the early development of sorghum and found that dramatic changes occur in shoot architecture during the early vegetative stages. Changes were observed in leaf size, leaf shape, numbers of trichomes, and size of the shoot apical meristem. In particular, the length/width ratios of the leaf blades in the fifth and upper leaves were completely different from those of the second to fourth leaves. The fifth and upper leaves have trichomes on their adaxial sides, which were absent on the lower leaves. We also analyzed expression of two microRNAs that are known to be molecular markers of the JA phase transition and found that expression of miR156 was highest in the second to fourth leaves and then was gradually down-regulated, whereas miR172 expression followed the opposite pattern. These results suggest that in sorghum, the second and third leaves represent the juvenile phase, the fourth and fifth leaves are in the transition stage, and the sixth and upper leaves are in the adult phase. Thus, the JA phase transition occurs during the fourth and fifth leaf stages. These findings are expected to be useful for understanding the early development of sorghum.
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Abbreviations
- DAG:
-
Days after germination
- JA:
-
Juvenile-to-adult
- miRNA:
-
MicroRNA
- qRT-PCR:
-
Quantitative RT-PCR
- SAM:
-
Shoot apical meristem
References
Agarwal T, Grotewold E, Doseff AI, Gray J (2016) MYB31/MYB42 syntelogs exhibit divergent regulation of phenylpropanoid genes in Maize, Sorghum and Rice. Sci Rep 6:28502. https://doi.org/10.1038/srep28502
Asai K, Satoh N, Sasaki H, Satoh H, Nagato Y (2002) A rice heterochronic mutant, mori1, is defective in the juvenile-adult phase change. Development 129(1):265–273
Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15(11):2730–2741. https://doi.org/10.1105/tpc.016238
Bassiri A, Irish EE, Poethig RS (1992) Heterochronic effects of Teopod 2 on the growth and photosensitivity of the Maize Shoot. Plant Cell 4(4):497–504. https://doi.org/10.1105/tpc.4.4.497
Bongard-Pierce DK, Evans MMS, Poethig RS (1996) Heteroblastic features of leaf anatomy in maize and their genetic regulation. Int J Plant Sci 157(4):331–340
Chuck G, Cigan AM, Saeteurn K, Hake S (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39(4):544–549. https://doi.org/10.1038/ng2001
Chuck GS, Tobias C, Sun L, Kraemer F, Li C, Dibble D, Arora R, Bragg JN, Vogel JP, Singh S, Simmons BA, Pauly M, Hake S (2011) Overexpression of the maize Corngrass1 microRNA prevents flowering, improves digestibility, and increases starch content of switchgrass. Proc Natl Acad Sci USA 108(42):17550–17555. https://doi.org/10.1073/pnas.1113971108
Clark LE (1970) Embryonic leaf number in sorghum. Crop Sci 10(3):307–309
Dien BS, Sarath G, Pedersen JF, Sattler SE, Chen H, Funnell-Harris DL, Nichols NN, Cotta MA (2009) Improved sugar conversion and ethanol yield for forage sorghum (Sorghum bicolor L. Moench) lines with reduced lignin contents. Bioenergy Res 2(3):153–164. https://doi.org/10.1007/s12155-009-9041-2
Dudley M, Poethig RS (1993) The heterochronic Teopod1 and Teopod2 mutations of maize are expressed non-cell-autonomously. Genetics 133(2):389–399
Evans MM, Poethig RS (1995) Gibberellins promote vegetative phase change and reproductive maturity in maize. Plant Physiol 108(2):475–487
Evans MM, Passas HJ, Poethig RS (1994) Heterochronic effects of glossy15 mutations on epidermal cell identity in maize. Development 120(7):1971–1981
Hibara K, Isono M, Mimura M, Sentoku N, Kojima M, Sakakibara H, Kitomi Y, Yoshikawa T, Itoh J, Nagato Y (2016) Jasmonate regulates juvenile-to-adult phase transition in rice. Development 143(18):3407–3416. https://doi.org/10.1242/dev.138602
Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46(1):23–47. https://doi.org/10.1093/pcp/pci501
Lauter N, Kampani A, Carlson S, Goebel M, Moose SP (2005) microRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc Natl Acad Sci USA 102(26):9412–9417. https://doi.org/10.1073/pnas.0503927102
Lawson JE, Poethig RS (1995) Shoot development in plants: time for a change. Trends Genet 11(7):263–268
Liu WY, Chang YM, Chen SC, Lu CH, Wu YH, Lu MY, Chen DR, Shih AC, Sheue CR, Huang HC, Yu CP, Lin HH, Shiu SH, Ku MS, Li WH (2013) Anatomical and transcriptional dynamics of maize embryonic leaves during seed germination. Proc Natl Acad Sci USA 110(10):3979–3984. https://doi.org/10.1073/pnas.1301009110
Moose PS, Sisco HP (1996) Glossy15, an APETALA2-1ike gene from maize that regulates leaf epidermal cell identity. Genes Dev 10(23):3018–3027
Moose SP, Lauter N, Carlson SR (2004) The maize macrohairless1 locus specifically promotes leaf blade macrohair initiation and responds to factors regulating leaf identity. Genetics 166(3):1451–1461
Moreno MA, Harper LC, Krueger RW, Dellaporta SL, Freeling M (1997) liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes Dev 11(5):616–628. https://doi.org/10.1101/gad.11.5.616
Ordonio RL, Ito Y, Hatakeyama A, Ohmae-Shinohara K, Kasuga S, Tokunaga T, Mizuno H, Kitano H, Matsuoka M, Sazuka T (2014) Gibberellin deficiency pleiotropically induces culm bending in sorghum: an insight into sorghum semi-dwarf breeding. Sci Rep 4:5287. https://doi.org/10.1038/srep05287
Orkwiszewski JA, Poethig RS (2000) Phase identity of the maize leaf is determined after leaf initiation. Proc Natl Acad Sci USA 97(19):10631–10636. https://doi.org/10.1073/pnas.180301597
Ozawa S, Hatakeyama K, Takahata Y, Yokoi S, Morris B (2017) The transition time from the juvenile phase to the adult phase differs in soybean cultivars ‘Enrei’ and ‘Peking’. Plant Breed 136(3):386–392. https://doi.org/10.1111/pbr.12476
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob ur R, Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457(7229):551–556. https://doi.org/10.1038/nature07723
Perazza D, Vachon G, Herzog M (1998) Gibberellins promote trichome formation by up-regulating GLABROUS1 in arabidopsis. Plant Physiol 117(2):375–383. https://doi.org/10.1104/pp.117.2.375
Poethig RS (2013) Vegetative phase change and shoot maturation in plants. Curr Top Dev Biol 105:125–152. https://doi.org/10.1016/B978-0-12-396968-2.00005-1
Quinby JR, Karper RE (1954) Inheritance of height in sorghum. Agron J 46:211–216
Sylvester AW, Parker-Clark V, Murray GA (2001) Leaf shape and anatomy as indicators of phase change in the grasses: comparison of maize, rice, and bluegrass. Am J Bot 88(12):2157–2167
Tanaka N, Itoh H, Sentoku N, Kojima M, Sakakibara H, Izawa T, Itoh J, Nagato Y (2011) The COP1 ortholog PPS regulates the juvenile-adult and vegetative-reproductive phase changes in rice. Plant Cell 23(6):2143–2154. https://doi.org/10.1105/tpc.111.083436
Telfer A, Bollman MK, Poethig RS (1997) Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 124(3):645–654
Wang H, Wang H (2015) The miR156/SPL module, a regulatory hub and versatile toolbox, gears up crops for enhanced agronomic traits. Mol Plant 8(5):677–688. https://doi.org/10.1016/j.molp.2015.01.008
Wang JW, Park MY, Wang LJ, Koo Y, Chen XY, Weigel D, Poethig RS (2011) miRNA control of vegetative phase change in trees. PLoS Genet 7(2):e1002012. https://doi.org/10.1371/journal.pgen.1002012
Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133(18):3539–3547. https://doi.org/10.1242/dev.02521
Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138(4):750–759. https://doi.org/10.1016/j.cell.2009.06.031
Xiao K, Mao X, Lin Y, Xu H, Zhu Y, Cai Q, Xie H, Zhang J (2017) Trichome, a functional diversity phenotype in plant. Mol Biol 6(1):183. https://doi.org/10.4172/2168-9547.1000183
Yang L, Xu M, Koo Y, He J, Poethig RS (2013) Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. Elife 2:e00260. https://doi.org/10.7554/eLife.00260
Yoshikawa T, Ozawa S, Sentoku N, Itoh J, Nagato Y, Yokoi S (2013) Change of shoot architecture during juvenile-to-adult phase transition in soybean. Planta 238(1):229–237. https://doi.org/10.1007/s00425-013-1895-z
Yu N, Cai WJ, Wang S, Shan CM, Wang LJ, Chen XY (2010) Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 22(7):2322–2335. https://doi.org/10.1105/tpc.109.072579
Yu S, Cao L, Zhou CM, Zhang TQ, Lian H, Sun Y, Wu J, Huang J, Wang G, Wang JW (2013) Sugar is an endogenous cue for juvenile-to-adult phase transition in plants. Elife 2:e00269. https://doi.org/10.7554/eLife.00269
Acknowledgements
This work was partially funded by JSPS KAKENHI Grant Number 18K05578 (S.Y.). Plant materials were kindly provided by Dr. Shigemitsu Kasuga at Shinshu University.
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SH and SY conceived and designed the research. SH conducted all the experiments. SH and SY analyzed the data and SH and SY wrote the manuscript. All authors read and approved the manuscript.
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Hashimoto, S., Tezuka, T. & Yokoi, S. Morphological changes during juvenile-to-adult phase transition in sorghum. Planta 250, 1557–1566 (2019). https://doi.org/10.1007/s00425-019-03251-x
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DOI: https://doi.org/10.1007/s00425-019-03251-x