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First published online April 30, 2004; 10.1104/pp.104.039453 Plant Physiology 135:201-211 (2004) © 2004 American Society of Plant Biologists Extensive Phenotypic Variation in Early Flowering Mutants of Arabidopsis1Laboratoire de Biologie Cellulaire, Institut National de la Recherche Agronomique, F78026 Versailles cedex, France
Flowering time, the major regulatory transition of plant sequential development, is modulated by multiple endogenous and environmental factors. By phenotypic profiling of 80 early flowering mutants of Arabidopsis, we examine how mutational reduction of floral repression is associated with changes in phenotypic plasticity and stability. Flowering time measurements in mutants reveal deviations from the linear relationship between the number of leaves and number of days to bolting described for natural accessions and late flowering mutants. The deviations correspond to relative early bolting and relative late bolting phenotypes. Only a minority of mutants presents no detectable phenotypic variation. Mutants are characterized by a broad release of morphological pleiotropy under short days, with leaf characters being most variable. They also exhibit changes in phenotypic plasticity across environments for florigenic-related responses, including the reaction to light and dark, photoperiodic behavior, and Suc sensitivity. Morphological pleiotropy and plasticity modifications are differentially distributed among mutants, resulting in a large diversity of multiple phenotypic changes. The pleiotropic effects observed may indicate that floral repression defects are linked to global developmental perturbations. This first, to our knowledge, extensive characterization of phenotypic variation in early flowering mutants correlates with the reports that most factors recruited in floral repression at the molecular genetic level correspond to ubiquitous regulators. We discuss the importance of functional ubiquity for floral repression with respect to robustness and flexibility of network biological systems.
Mutational analyses have proved very useful to identify gene functions (Bouché and Bouchez, 2001  ; Alonso et al., 2003). In turn, the realization that gene functions are involved in reticulate networks of interactions contributed to the emergence of systems biology that is based on exhaustive, simultaneous biological descriptions (Katagiri, 2003). Network systems reveal emergent properties that cannot be predicted from the properties of isolated constituents but are specific of the interactive whole. In particular, the intricacy and flexibility of complex interactions indicates that gene functions are not only primary causal agents of specific processes but can also be recruited directly or indirectly in different processes of a system (Duboule and Wilkins, 1998; Greenspan, 2001). This functional versatility suggests that mutant phenotypes reflect not only specific functional effects but also distortions of wild-type network systems. Canalization or robustness, the capacity of network biological systems to buffer a wide variety of perturbations (Waddington, 1942; Rutherford, 2000; Debat and David, 2001; Siegal and Bergman, 2002) can explain why numerous silent mutations are uncovered in insertion mutagenesis analyses (Bouché and Bouchez, 2001). But mutants are usually less canalized than wild types, and most mutations can affect the expression of numerous unrelated genes and reveal multiple phenotypic variations (Waddington, 1942; Duboule and Wilkins, 1998; Rutherford, 2000; Wagner, 2000; Finnegan, 2001; Greenspan, 2001; Featherstone and Broadie, 2002; Bergman and Siegal, 2003). The degree of pleiotropy and distribution of phenotypic variation in mutants should thus help to characterize robustness and flexibility of network biological systems.
Both robustness and flexibility are crucial properties of network systems that allow developmental stability while enhancing coordinate, orderly dynamic variation necessary for growth and adjustment to the environment (Greenspan, 2001
Mutant lines have been mostly used by developmental biologists for molecular genetic analyses, but the impact of mutations on phenotypic plasticity and pleiotropy has not been well studied (Bagnall, 1993
Altered Rates of Progression to Flowering
In an initial screen for early flowering mutants under short days (SD), 81 mutants in Ws and Col-0 ecotypes were selected for further analysis (Pouteau et al., 2001
Diversity in Morphological Pleiotropy
To recover the widest range of phenotypic effects associated with early flowering, the only phenotypic selection applied in the initial screen, apart from flowering time, was based on fertility and uniformity of transmission. Strikingly, the mutants exhibit a large range of morphological modifications, such as changes in plant architecture, modified leaf morphology, or altered pigmentation (Fig. 2). An example of a highly pleiotropic phenotype was described for the lhp1-1 and lhp1-2 mutants, including dramatic changes in plant architecture and leaf morphology, as well as dwarfism (Gaudin et al., 2001
The range of morphological variation in the mutants under SD was investigated by a phenomenological survey at different developmental stages. We identified 28 variable morphological parameters ranging from vegetative features (for example elongation of petiole and hypocotyl) to floral and inflorescence features (Fig. 3). Only four mutants have no macroscopic morphological modification, and the level of morphological pleiotropy per mutant (estimated as the percentage of modified morphological parameters) is 24.5% on average. A large diversity is observed in the distribution of the variation among mutants (Fig. 3A). Each level of morphological variation (0–16 modifications per mutant) is equally represented in the population of mutants, suggesting that the range of possible multiple morphological changes is not limited.
The 28 variable parameters are characterized by contrasting frequencies of variation in the mutant population. The variation level is highest for rosette pigmentation and rosette leaf shape (more than 60% of the mutants) and lowest for floral features, silique shape, and elongation of secondary inflorescences (less than 10% of the mutants; Fig. 3B). Changes in rosette leaf shape and pigmentation may be respectively associated with modifications in the leaf heteroblastic transition due to reduction in the number of leaves or temporal changes and perturbations either in photosynthesis and growth capacity or in light perception and signaling. The distribution of the level of morphological pleiotropy with flowering time also shows a wide range of variation among mutants (Fig. 2J). Most of the earliest mutants (less than 20 leaves) are highly pleiotropic while moderately early mutants (between 20 and 30 leaves) exhibit more variable levels of pleiotropy.
Gene tagging analysis indicates that morphological pleiotropy and early flowering are genetically linked in the T-DNA insertion mutants. The average frequency of tagging by a T-DNA expressing kanamycin resistance is 31%. This suggests that each T1 parental line potentially bears three or four mutations. Yet, analyses of F2 and T2 populations for 52 T-DNA insertion mutants reveal no phenotypic segregation of the mutant features. This suggests that only one locus is affected in these mutants. The frequency of linkage is higher in T2 lines having two independent T-DNA insertion loci (55%) than in T2 lines having one single T-DNA insertion locus (28%). Multiple insertion may reflect a higher efficiency and lower rate of abortion of the T-DNA insertion process. Indeed, part of the nontagged mutants are probably due to point mutations caused by aborted insertion. In total 16 mutants show linkage between early flowering and a T-DNA insertion, and for 12 of them the genetic distance is less than 1%. Despite potentially different underlying mechanisms, no significant difference is observed in the phenotypic behavior of semidominant (11) and recessive (49) T-DNA insertion mutants. Based on morphological similarities, alleles could only be detected for five complementation groups, each of them comprising no more than two or three alleles. Comparison between alleles reveals no significant difference in their phenotypic variation. Over 100 random crosses in a sample population of 24 mutants all resulted in complementation. This suggests that in the absence of morphological similarities allelism is rare and that many mutants in the collection are probably unique members of their corresponding complementation group. The large phenotypic diversity in the collection is thus reflected by a low level of genetic redundancy. Because of this lack of redundancy, it is likely that the collection is not saturated and that the number of loci associated with floral repression is high.
To further characterize the phenotypic pleiotropy of early flowering mutants, their norms of reaction were assayed in response to environmental constraints having a florigenic influence. Two levels of the regulation of flowering time by photoperiod were investigated (Millar, 1999
Comparison between the two genetic backgrounds shows that Ws is more sensitive to paclobutrazol than Col-0. Ws germination is fully inhibited at a concentration of 3 x 10–5 M while Col-0 still exhibits residual resistance at a concentration of 3 x 10–4 M (1.65% ± 1.23%). Mutants in the two genetic backgrounds also show a differential response to paclobutrazol. No resistance is detected for 61 mutants in the Ws background, while 3 out of 13 mutants in the Col-0 background exhibit a significant decrease in sensitivity (data not shown). The different flexibility of the response to paclobutrazol in the two ecotypes may indicate that mutational effects on phenotypic variation are potentially bound to parental limitations. This may be tentatively explained by the fact that Ws is genetically constrained by a defect in phytochrome D and is an early flowering mutant itself (Auckerman et al., 1997
Norms of Reaction to Photoperiod
Norms of Reaction to Light and Dark Hypocotyl elongation was determined in classical dark and LD light conditions and, for a number of mutants, in SD light condition. In Ws and Col-0 wild types, hypocotyl elongation is repressed in the light and is strongly activated in the dark (Gendreau et al., 1997 ). For Ws, no significant difference is observed in the two light conditions, but the kinetics of hypocotyl elongation is slower in SD than in LD (data not shown). For about two-thirds of the T-DNA insertion mutants, hypocotyl elongation is significantly different from the wild type in at least one of the conditions tested. However, only seven mutants are affected in both light and dark conditions, and six mutants exhibit changes only in SD but not in LD. Six classes of response to light and dark based on hypocotyl elongation can be identified: class Hyp1, long in light; class Hyp2, long in light and short in dark; class Hyp3, short in light; class Hyp4, short in light and in dark; class Hyp5, short in dark; and class HypN, similar to the wild type (Fig. 5). Similar results were obtained in EMS mutants: among 10 mutants analyzed, only one is similar to the wild type and two are affected in both light and dark conditions (data not shown).
Norms of Reaction to Suc For Ws and Col-0, the presence of 6% Suc delays germination and early development but subsequent development is little affected. The mutant behavior on 0% Suc is not significantly different from the wild type. We identified four classes of sensitivity to 6% Suc in the T-DNA insertion mutants (Fig. 5; see "Materials and Methods"). Class Suc1 exhibits a high level of early growth arrest (up to 64%) so that only a small proportion of seedlings develop into adult plants, a marked accumulation of anthocyanin and epinasty. For class Suc2, early growth arrest is limited and a majority of seedlings develop into adult plants characterized by a high level of shoot and leaf distortion and anthocyanin accumulation. Finally, class Suc3 shows only weak or variable germination or developmental defects, and class SucN is similar to the wild type.
The mutants are characterized by a large diversity in the distribution of the different norms of reaction (Fig. 5, A and B). Multiple changes in response to photoperiod (P), Suc hypersensitivity (S), and hypocotyl elongation (H) are more frequent than single changes (Fig. 5C). To estimate the distribution of phenotypic plasticity with flowering time, P, S, and H phenotypic indices were calculated and used to determine a global plasticity index Pi (0.66 on average in the mutant population). The indices appear differentially distributed in the different categories of mutants (Table I; Fig. 6). Despite a wide range of variation among the mutants, Pi tends to be lower with earlier flowering time, and some categories of mutants localize to different sectors of this distribution.
In most cases, S is associated with P and H together, suggesting that it reflects global developmental perturbation (Fig. 5C). Accordingly, classes Suc1-3 comprising the relative late bolting subpopulation are characterized by a low Pi. Because of their moderately early flowering time, they account for the main deviation from a putative linear relation between flowering time and plasticity in the mutant population (Fig. 6A). S is most often combined with class PhP3 and classes Hyp1 to Hyp4 (14 out of 17 mutants in both cases). The H index decreases from class Suc1 to SucN, supporting the possibility of a positive correlation between H and S. In contrast, the P index is not significantly different in the different Suc classes, suggesting that the correlation between P and S is indirect (Table I; data not shown). P and H are combined in 50% of the mutants (Fig. 5C). A positive correlation between P and H is suggested by the fact that the H index decreases from class PhP1 to PhP4 and that the P index is higher in classes Hyp1 to Hyp4 and intermediate in class Hyp5 compared to class HypN (Table I). The variation in P and H indices is reflected in the distribution of Pi variation with flowering time (Fig. 6, B and C). Classes PhP1-2 and class PhP4 correspond to two separate clusters comprising, respectively, the earliest mutants with a low Pi and most of the least precocious mutants with highest Pi. In contrast, class PhP3 and most Hyp classes do not localize to a specific sector. However, most mutants in classes Hyp1 to Hyp4 have a low Pi, whereas class Hyp5 exhibits an intermediate Pi and is clustered near class HypN characterized by the highest Pi.
According to a mechanistic understanding of photoperiodism, P and H alterations can reveal a reduced capacity to integrate environmental cues at the input level, including light photoreception and signaling, or at the oscillator or output levels due to clock dysfunction (Samach and Coupland, 2000
Based on the first, to our knowledge, extensive characterization of early flowering mutants in Arabidopsis, our work provides new perspectives on the regulation of floral repression in relation to phenotypic variation. First, early flowering mutants exhibit modifications in the coordination of two temporal components of plant ontogeny: an exogenous component corresponding to environmental timing measured by the date of flowering, and an endogenous component related to organismic timing estimated by the number of leaves. The uncoupling of these two components results in relative early or late bolting phenotypes. In contrast, most previous analyses conducted with late flowering mutants or natural accessions and RILs indicated a strong correlation between the date of flowering and the number of leaves (Koornneef et al., 1991 ; Bagnall, 1993; Karlsson et al., 1993; Clarke et al., 1995; Kuittinen et al., 1997; Stratton, 1998). The difference in the behavior of early and late flowering mutants may be explained by the fact that the latter had been selected for a lack of pleiotropic effects (M. Koornneef, personal communication). A comparison of the early flowering mutants with late flowering mutants not submitted to a phenotypic selective bias would thus be interesting. Because the relative late bolting phenotypes are most affected, it is possible that uncoupling of the two temporal dimensions in late flowering mutants would also be associated with profound disruptions of developmental stability. However, the high level of phenotypic variation in early flowering mutants is probably not coincidental with the type of selection applied but reflects endogenous constraints imposed by advanced ontogenetic phase change (see below). In addition, the uncoupling of endogenous and exogenous temporal components in relative early bolting phenotypes could reflect a slower rate of leaf initiation at early stages (Groot and Meicenheimer, 2000). Additional growth rate measurements would be needed to discriminate between different possible modes of variation in flowering time (Wiltshire et al., 1994; Diggle, 1999).
Second, early flowering mutants exhibit extensive phenotypic variation. This is characterized by a release of morphological pleiotropy under SD and a decrease in phenotypic plasticity across environments resulting in multiple variation profiles. Among the 28 variable morphological parameters identified, leaf characters are most often affected. The lower level of variation observed for floral features may be coincidental with the selection for fertility applied during the mutant screen. But this may also reflect their higher robustness against variation due to their more determinate character. Conversely, vegetative features may be more variable because of their higher flexibility as reflected by heteroblasty, i.e. the gradual change in leaf morphology exhibited by regular ontogenetic sequences (Diggle, 1999
Third, the high level of pleiotropy in early flowering mutants emphasizes the importance of functional ubiquity for the interpretation of floral repression at the molecular genetic level. Indeed, floral repression seems to have recruited more ubiquitous factors than floral activation, including members of the MADS-box gene superfamily that act through complex multimeric protein interactions and epigenetic regulators (Goodrich et al., 1997
By integrating a growing number and complexity of regulatory factors, the current genetic models have substantially contributed to advancing our understanding of flowering time in Arabidopsis. More recently attempts have been made to include some repressors in regulatory networks, for example FLC and EFS (Michaels and Amasino, 1999
Plant Material
T-DNA insertion lines of Wassilewskija (Ws) ecotype were obtained from the Versailles collection, INRA, France (Bechtold et al., 1993
Mutant seeds were sown on soil (Stender A240, Blumenerdenwerk Stender, Schermbeck, Germany) and grown in Sanyo Gallenkamp SGC660 growth cabinets at 20 ± 0.2°C and 70% ± 2% relative humidity. The soil was kept moist by application of nutrient solution three times a week. The light was provided by mixed fluorescent and incandescent tubes and the photon flux density (PFD) measured at soil level was 230 ± 20 µE m–2 s–1 and 2 ± 0.2 µE m–2 s–1, respectively. SD corresponded to 8 h light and 16 h dark, and LD conditions consisted of 16 h light and 8 h dark. Developmental uniformity was obtained by selecting the 10 most uniform plants on average about 12 d after sowing, bringing the plant density to one plant per pot, and rotating the trays three times a week. Bolting time was measured as the number of days from sowing to the first elongation of the floral stem at 0.1 cm height. The number of true leaves produced by the apical meristem was recorded on bolted plants. No major variation was observed in two to four independent repeats (12 repeats in SD and 9 in LD for Ws).
Repeated characterizations of mutant phenotypes under SD in successive generations obtained from the initial screen and in genetic analyses were further investigated in an exhaustive survey. Four individuals per genotype were selected for developmental uniformity and grown in parallel in the same growth room in SD. Aerial morphological features (vegetative, floral, inflorescence, and plant architecture) were examined after 4 and 10 weeks. Apart from floral features that were observed under a dissection microscope, all parameters were macroscopically recorded. Size or quantity parameters were semiquantified by recording the corresponding ranges of variation for each genotype compared to the wild type. The other parameters such as fertility or leaf surface wrinkling were visually assessed on a qualitative basis.
Mutant seeds were sterilized and sown on petri dishes containing a standard nutrient medium as described by Santoni et al. (1994)
For hypocotyl length measurements, seedlings were grown on standard nutrient medium without Suc during 10 d for LD and dark conditions according to Gendreau et al. (1997) For Suc sensitivity measurements, seedlings were grown on standard nutrient medium without Suc or with 6% (w/v) Suc. Germination and early development were recorded at different times during a period of 3 to 17 d of growth. Early development was divided into three stages: root emergence (stage 1); shoot emergence (stage 2); and cotyledon expansion and greening (stage 3). Later developmental stages, recorded as stage 3, were examined for morphological features in the initial population and in a subpopulation transferred to fresh medium after 10 to 15 d of growth. The sensitivity of the mutants to 6% Suc was determined by measuring the following parameters: inhibition of germination, early growth arrest (at stage 1 or stage 2), developmental delay (later transition from stage 1 to stage 2 and stage 3), morphological features including shoot or leaf distortion, anthocyanin accumulation, epinasty, and root phenotype. An average of 80 to 100 seeds was analyzed per genotype and per repeat. A consistent behavior was observed in two to four independent repeats performed for 34 mutants comprising all mutants exhibiting sensitivity to 6% Suc (10 repeats for the wild type). For paclobutrazol resistance assays, an average of 80 to 100 seeds was sown per genotype and per repeat on a 0.7% agar medium containing paclobutrazol (Sopra s.a., Zeneca Agrochemicals, Vélizy-Villacoublay, France) and the percentage of germination was scored after 7 to 10 d in LD. Mutant seeds in Ws and Col-0 backgrounds were assayed at a concentration of 10–5 to 3 x 10–5 M and 3 x 10–4 M paclobutrazol, respectively. Ws and Col-0 responses were assayed in five and four independent repeats, respectively.
The PSI was determined as the ratio between the total number of leaves in SD and the total number of leaves in LD. To estimate the deviations of the mutants from the corresponding wild-type plasticity response to photoperiod, Suc, and light/dark, P, S, and H phenotypic indices were calculated. Each index was based on three criteria analyzed: (P1) early in LD, (P2) reduced PSI, (P3) photoperiod insensitive (PSI approximately 1); (S1) morphological modifications and/or developmental delay, (S2) moderate inhibition of development (10%–30% early growth arrest), (S3) strong inhibition of development (50%–65% early growth arrest); and (H1) modification in LD, (H2) modification in SD, (H3) modification in the dark. Each criterion was given a value of 0 or 1 depending on the absence or presence of a significant difference with the wild type based on t test scores. The P, S, and H phenotypic indices were used to calculate a Pi plasticity index: Pi = [9 – (P + S + H)]/9.
We thank Hervé Ferry, Jean-Marie Pollien, and Joël Talbotec for technical assistance with plant culture and glasshouse work and Benoît Lacroix, Virginie Léon, and Cécile Marchenay for their help as trainee students. We are thankful to Nicole Bechtold, Georges Pelletier, and Roger Voisin for providing T-DNA insertion lines of the Versailles collection and to Catherine Bellini for the gift of EMS mutagenized lines. We are grateful to Yves Chupeau for his support and to Nissim Amzallag, Sylvie Dinant, Jean-Louis Durand, Herman Höfte, Jan Traas, Hervé Vaucheret, and Johannes Wirz for comments on this manuscript. Received January 19, 2004; returned for revision February 19, 2004; accepted February 25, 2004.
1 This work, V.F., and F.P. were supported by the European Union (grant no. BI04–CT97–2340). G.Z. received a Chinese Government fellowship. 
2 Present address: Physiologie Cellulaire et Moléculaire des Plantes, Université Pierre et Marie Curie, 4 Place Jussieu, F75252 Paris cedex 05, France.
3 Present address: Department of Plant Sciences, University of Oxford, South Park Road, Oxford OX1 3RB, UK.
4 Present address: College of Life Science and Biotechnology, Shanghai JiaoTong University, Mihang Dongchuan Road 800, Shanghai 200240, China. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.039453. * Corresponding author; e-mail sylvie.pouteau{at}versailles.inra.fr; fax 33–0–1–30833099.
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