Model-assisted physiological analysis of Phyllo, a rice architectural mutant
Delphine Luquet A D , You Hong Song B , Sonia Elbelt A , Dominique This C , Anne Clément-Vidal A , Christophe Périn A , Denis Fabre A and Michael Dingkuhn AA CIRAD, Amis Dpt, TA40/01 Avenue Agropolis, 34 398 Montpellier Cedex 5, France.
B Institute of Botany, the Chinese Academy of sciences, 100 093, Beijing, China.
C Ecole Nationale Supérieure Agronomique de Montpellier, UMR 1096, 2, place P. Viala, 34 060 Montpellier Cedex, France.
D Corresponding author. Email: luquet@cirad.fr
Functional Plant Biology 34(1) 11-23 https://doi.org/10.1071/FP06180
Submitted: 24 July 2006 Accepted: 11 October 2006 Published: 19 January 2007
Abstract
Studies of phenotype of knockout mutants can provide new insights into physiological, phenological and architectural feedbacks in the plant system. Phyllo, a mutant of Nippon Bare rice (Oryza sativa L.) producing small leaves in rapid succession, was isolated during multiplication of a T-DNA insertion library. Phyllo phenotype was compared with the wild type (WT) during vegetative development in hydroponics culture using a wide range of physiological and biometric measurements. These were integrated with the help of the functional–structural model EcoMeristem, explicitly designed to study interactions between morphogenesis and carbon assimilation. Although the phenotype of the mutant was caused by a single recessive gene, it differed in many ways from the WT, suggesting a pleiotropic effect of this mutation. Phyllochron was 25 (1–4 leaf stage) to 38% (>>4 leaf stage) shorter but showed normal transition from juvenile to adult phase after leaf 4. Leaf size also increased steadily with leaf position as in WT. The mutant had reduced leaf blade length : width and blade : sheath length ratios, particularly during the transition from heterotrophic to autotrophic growth. During the same period, root : shoot dry weight ratio was significantly diminished. Specific leaf area (SLA) was strongly increased in the mutant but showed normal descending patterns with leaf position. Probably related to high SLA, the mutant had much lower light-saturated leaf photosynthetic rates and lower radiation use efficiency (RUE) than the WT. Leaf extension rates were strongly reduced in absolute terms but were high in relative terms (normalised by final leaf length). The application of the EcoMeristem model to these data indicated that the mutant was severely deficient in assimilate, resulting from low RUE and high organ initiation rate causing high assimilate demand. This was particularly pronounced during the heterotrophic–autotrophic transition, probably causing shorter leaf blades relative to sheaths, as well as a temporary reduction of assimilate partitioning to roots. The model accurately simulated the mutant’s high leaf mortality and absence of tillering. The simulated assimilate shortage was supported by observed reductions in starch storage in sheaths. Soluble sugar concentrations differed between mutant and WT in roots but not in shoots. Specifically, the hexose : sucrose ratio was 50% lower in the roots of the mutant, possibly indicating low invertase activity. Furthermore, two OsCIN genes coding for cell wall invertases were not expressed in roots, and others were expressed weakly. This was interpreted as natural silencing via sugar signalling. In summary, the authors attributed the majority of observed allometric and metabolic modifications in the mutant to an extreme assimilate shortage caused by hastened shoot organogenesis and inefficient leaf morphology.
Additional keywords: cell-wall invertase, EcoMeristem model, leaf photosynthetic rate, T-DNA insertion mutant, Oryza sativa, phyllochron, source–sink relationships, sugar metabolism.
Acknowledgements
The authors wish to express their gratitude to the French Ministry for Foreign Affairs for financial support of a post-doctoral project.
An G,
Jeong D-H,
Jung K-H, Lee S
(2005) Reverse genetic approaches for functional genomics of rice. Plant Molecular Biology 59, 111–123.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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, 265–273.
| PubMed |
Asch F,
Sow A, Dingkuhn M
(1999) Reserve mobilization, dry matter partitioning and specific leaf area in seedlings of African rice cultivars differing in early vigor. Field Crops Research 62, 191–202.
| Crossref | GoogleScholarGoogle Scholar |
Bos HJ, Neuteboom JH
(1998) Morphological analysis of leaf and tiller dynamics of wheat (Triticum aestivum L.): responses to temperature and light intensity. Annals of Botany 81, 131–139.
| Crossref | GoogleScholarGoogle Scholar |
Cho JI,
Lee SK,
Ko S,
Kim H-K, Jun S-H ,
et al
.
(2005) Molecular cloning and expression analysis of the cell wall invertase gene family in rice (Oryza sativa L.). Plant Cell Reports 24, 225–236.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dingkuhn M,
Jones MP,
Johnson DE, Sow A
(1998) Growth and yield potential of Oryza sativa and O. glaberrima upland rice cultivars and their interspecific progenies. Field Crops Research 57, 57–69.
| Crossref | GoogleScholarGoogle Scholar |
Dingkuhn M,
Luquet D,
Quilot B, Reffye PD
(2005) Environmental and genetic control of morphogenesis in crops: towards models simulating phenotypic plasticity. Australian Journal of Agricultural Research 56, 1289–1302.
| Crossref | GoogleScholarGoogle Scholar |
Dingkuhn M,
Luquet D,
Kim HK,
Tambour L, Clément-Vidal A
(2006) EcoMeristem, a model of morphogenesis and competition among sinks in rice: 2. Simulating genotype responses to phosphorus deficiency. Functional Plant Biology 33, 325–337.
| Crossref | GoogleScholarGoogle Scholar |
Dubcovsky J
(2004) Marker-assisted selection in public breeding programs: the wheat experience. Crop Science 44, 1895–1898.
Fabre D,
Siband P, Dingkuhn M
(2005) Characterizing stress effects on rice grain development and filling using grain weight and size distribution. Field Crops Research 92, 11–16.
| Crossref | GoogleScholarGoogle Scholar |
Fiorani F,
Beemster GTS,
Bultynck L, Lambers H
(2000) Can meristematic activity determine variation in leaf size and elongation rate among four Poa species? A kinematic study. Plant Physiology 124, 845–856.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Foo E,
Turnbull CGN, Beveridge CA
(2001) Long-distance signaling and the control of branching in the rms1 mutant of pea. Plant Physiology 126, 203–209.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Frantz JM,
Pinnock D,
Klassen S, Bugbee B
(2004) Characterizing the environmental response of a gibberellic acid deficient rice for use as a model crop. Agronomy Journal 96, 1172–1181.
Frey JE,
Frey B,
Sauer C, Kellerhals M
(2004) Efficient low-cost DNA extraction and multiplex fluorescent PCR method for marker-assisted selection in breeding. Plant Breeding 123, 554–557.
| Crossref | GoogleScholarGoogle Scholar |
Hammer GL,
Kropff MJ,
Sinclair TR, Porter JR
(2002) Future contributions of crop modelling – from heuristics and supporting decision making to understanding genetic regulation and aiding crop improvement. European Journal of Agronomy 18, 15–31.
| Crossref | GoogleScholarGoogle Scholar |
Itoh JI,
Hasegawa A,
Kitano H, Nagato Y
(1998) A recessive heterochronic mutation, plastochron 1, shortens the plastochron and elongates the vegetative phase in rice. The Plant Cell 10, 1511–1521.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ji X,
Van den Ende W,
Van Laere A,
Cheng S, Bennett J
(2005) Structure, evolution, and expression of the two invertase gene families of rice. Journal of Molecular Evolution 60, 615–634.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kawakatsu T,
Itoh J,
Miyoshi K,
Kurata N,
Alvarez N,
Veit B, Nagato Y
(2006) PLASTOCHRON2 regulates leaf initiation and maturation in rice. The Plant Cell 18, 612–625.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kushiro T,
Okamoto M,
Nakabayashi K,
Yamagishi K,
Kitamura S,
Asami T,
Hirai N,
Koshiba T,
Kamiya Y, Nambara E
(2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. EMBO Journal 23, 1647–1656.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Li J, Chory J
(1999) Brassinosteroid actions in plants. Journal of Experimental Botany 50, 275–282.
| Crossref | GoogleScholarGoogle Scholar |
Liu F,
Jensen CR, Andersen MN
(2005) A review of drought adaptation in crop plants: changes in vegetative and reproductive physiology induced by ABA-based chemical signals. Australian Journal of Agricultural Research 56, 1245–1252.
| Crossref | GoogleScholarGoogle Scholar |
Luquet D,
Zhang B,
Dingkuhn M,
Dexet A, Clément-Vidal A
(2005) Phenotypic plasticity of rice seedlings: case of phosphorus deficiency. Plant Production Science 8, 145–151.
| Crossref | GoogleScholarGoogle Scholar |
Luquet D,
Dingkuhn M,
Kim HK,
Tambour L, Clément-Vidal A
(2006) EcoMeristem, a model of morphogenesis and competition among sinks in rice. 1. Concept, validation and sensitivity analysis. Functional Plant Biology 33, 309–323.
| Crossref | GoogleScholarGoogle Scholar |
Miyoshi K,
Ahn BO,
Kawakatsu T,
Ito Y,
Itoh JI,
Nagato Y, Kurata N
(2004) PLASTOCHRON1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. Proceedings of the National Academy of Sciences USA 101, 875–880.
| Crossref | GoogleScholarGoogle Scholar |
Nelder J, Mead R
(1965) A simplex method for function minimization. Computer Journal 7, 308–313.
Reymond M,
Muller B,
Leonardi A,
Charcosset A, Tardieu F
(2003) Combining quantitative trait loci analysis and an ecophysiological model to analyse the genetic variability of the responses of maize leaf growth to temperature and water deficit. Plant Physiology 131, 664–675.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roitsch T,
Ehne R,
Goetz M,
Hause B,
Hofmann M, Krishna Sinha A
(2000) Regulation and function of extracellular invertase from higher plants in relation to assimilate partitioning, stress responses and sugar signalling. Australian Journal of Plant Physiology 27, 815–825.
Roitsch T, Gonzales M
(2004) Function and regulation of plant invertases: sweet sensations. Trends in Plant Science 9, 606–613.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sallaud C,
Gay C,
Larmande P,
Bes M, Piffanelli P ,
et al
.
(2004) High throughput T-DNA insertion mutagenesis in rice: a first step towards in silico reverse genetics. The Plant Journal 39, 450–464.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tanabe S,
Ashikari M,
Fujioka S,
Takatsuto S, Yoshida S ,
et al
.
(2005) A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. The Plant Cell 17, 776–790.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tivet F,
da Silveira Pinheiro B,
de Raïssac M, Dingkuhn M
(2001) Leaf blade dimensions of rice (Oryza sativa L. and Oryza glaberrima Steud.). Relationships between tillers and main stem. Annals of Botany 88, 507–511.
| Crossref | GoogleScholarGoogle Scholar |
Werner T,
Motyka V,
Strnad M, Schmülling T
(2001) Regulation of plant growth by cytokinin. Proceedings of the National Academy of Sciences USA 98, 10487–10492.
| Crossref | GoogleScholarGoogle Scholar |
Xiong GS,
Hu XM,
Jiao YQ,
Yu YC,
Chu CC,
Li JY,
Qian Q, Wang YH
(2006) Leafy head2, which encodes a putative RNA-binding protein, regulates shoot development of rice. Cell Research 16, 267–276.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yin X,
Struik PC, Kropff MJ
(2004) Role of crop physiology in predicting gene-to-phenotype relationships. Trends in Plant Science 9, 426–432.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
