Crop Science 43:886-891 (2003)
© 2003 Crop Science Society of America
CROP PHYSIOLOGY & METABOLISM
Both Promoters and Inhibitors Affected Flowering Time in Grafted Soybean Flowering-Time Isolines
Elroy R. Cober*,a and
Daniel F. Curtisb
a Eastern Cereal and Oilseed Research Centre (ECORC), Agric. & Agri-Food Canada, Bldg. 110, Central Exp. Farm, Ottawa, ON, Canada, K1A 0C6
b Biofloral Inc., 38723 Fingal Line, RR#1, St. Thomas, ON, Canada, N5P 3S5
* Corresponding author (coberer{at}agr.gc.ca)
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ABSTRACT
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Understanding the control of flowering time in photoperiod-sensitive plants has been furthered by grafting experiments. In soybean [Glycine max (L.) Merr.], genes which control flowering time have been identified and their responses to photoperiod characterized. Grafting experiments allow the study of interactions between genotypes. The objective of our study was to characterize the flowering response of scions from a grafted series of early- to late-flowering soybean near-isogenic lines. Seedling scions were grafted to 1-wk-older rootstocks and grown under noninductive 16-h days. Rootstocks were allowed to develop a single axillary shoot to allow interaction between rootstock and scion shoots. Late-flowering rootstocks did not delay flowering of the earliest-flowering isolines but delayed flowering of intermediate-flowering isolines. Some floral inhibition was also seen within scions since defoliated late-flowering scions grafted to early-flowering rootstocks flowered earlier compared with nondefoliated scions of the same graft combination. Early-flowering rootstocks promoted flowering of late-flowering scions both within and across genetic backgrounds. Early-flowering scions flowered early (27 to 30 d) regardless of rootstock genotype. This early flowering was observed even when the scions were defoliated, indicating that floral promoters might be produced or sensed in unexpanded leaves or buds. The activity of floral promoters and inhibitors was demonstrated in soybean and these factors appeared to mediate flowering time antagonistically.
Abbreviations: MG, maturity group • PHY, phytochrome
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INTRODUCTION
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THE CONTROL OF floral initiation in plants has been studied for many years. Levy and Dean (1998) reviewed models for the control of flowering time including the florigen concept postulated by Chailakhyan (1936), the nutrient diversion model, and the current multifactorial control model. The specific mechanism of flower initiation may be unclear, but several experiments identified leaves as the site of photoperiod recognition and floral inhibitor production. Lang and Melchers (1943) demonstrated that long-day black henbane (Hyoscyamus niger L.) grown in noninductive short photoperiods flowered when all mature leaves were removed. The presence of a single mature leaf was sufficient to prevent flowering. A similar result was demonstrated in short-day plants using strawberry (Fragaria x ananassa Rozier). Strawberry plants, when partially defoliated of mature leaves, flowered under slightly noninductive photoperiods; when fully defoliated of mature leaves they showed no floral inhibition and flowered under a continuous photoperiod (Thompson and Guttridge, 1960). Withrow and Withrow (1943), using cocklebur [Xanthium pensylvanicum Wallr. (= Xanthium strumarium L.)], demonstrated that steaming of petioles restricted phloem transport and prevented flowering. These studies indicate that photoperiod recognition and floral regulation begins within mature leaves in both long and short day plants. However, Hopkinson and Ison (1982) reported that the flowering response of day-neutral and short-day tobacco plants was controlled in the new upper leaves and that removal of these leaves while allowing the lower mature leaves to stay intact prevented flowering. These contradictory reports would indicate that a generalized model for the site of flower promotion and inhibition may not be possible between long- and short-day species.
Grafting experiments have been instrumental in developing an understanding of floral inhibitors and promoters through observation of rootstock effects on scions. Mango (Mangifera indica L.) was stimulated to flower out of season with the addition of a leaf from a flowering mango plant (Kulkarni, 1986). Using pea (Pisum sativum L.), Murfet (1971) noted that scions, from six lines with different combinations of alleles at three loci controlling time to flowering, had a range of flowering responses varying between a 17-node promotion to an eight-node delay in flowering when grafted to various rootstocks. The author suggested that a floral inhibitor was produced in the cotyledons and leaves and that the genetic makeup of the lines controlled apical sensitivity to this inhibitor. The results also suggested that a floral promoter was produced by certain lines since there was up to a 17-node promotion of flowering time in some combinations. More recent work with pea showed the fun1 (far-red unresponsive) mutant, which lacks the phytochrome (PHY) A apoprotein and is also known as phyA, delayed flowering when grafted to wild-type plants even under strongly inductive conditions (Weller et al., 1997). Weller et al. (2001) also showed, using phyB mutants, that PHYB functions to inhibit flowering but that the inhibitor is not graft transmissible. In tobacco (Nicotiana tabacum L.), different genotypes can be short-day or day-neutral types and can be grafted to the closely related long-day species Nicotiana sylvestris Speg. & Comes. Lang et al. (1977) showed that long- and short-day scions hastened flowering of indicator shoots on day-neutral rootstocks when grown under the scion's respective inductive photoperiod. However, only the long-day scion was able to maintain vegetative growth when grafted to the day-neutral plant under noninductive photoperiods. These results show that both flower promotion and inhibition can be observed in plants and that they may compete in controlling flowering time.
In soybean, a short-day plant, genetic control of flowering and maturity has been well documented with the identification and description of genes which delay flowering under extended photoperiods (Bernard, 1971; Buzzell, 1971; Saindon et al., 1989; McBlain and Bernard, 1987; Cober and Voldeng, 2001). Under inductive short days, early- and later-flowering near-isogenic lines flower similarly and early. Differences in flowering times among these isolines only become apparent as the photoperiod increases (Cober et al., 2001). Soybean flowering, or more accurately, photoperiod-sensitivity genes seem to function to inhibit flowering under noninductive conditions.
Carver et al. (1987) showed that flowering of a scion from an early-maturing soybean plant was delayed when grafted to the rootstock of a late-maturing line. The early-maturing rootstock had no effect on the late-maturing scion. This contradicts other work where early-maturing rootstocks were able to induce flowering in scions from later-maturing lines. Heinze et al. (1942) reported that a photoperiod-insensitive cultivar, Agate, was able to induce flower buds on Biloxi, a late-maturing cultivar when joined in a graft union. Kiihl et al. (1977) and Beaver and Nelson (1981) found that scions from late-maturing plants, when grafted to early maturing rootstock, flowered earlier than ungrafted plants. An interesting result was reported by Newell and Hymowitz (1979) in which a wild accession, G. tomentella Hayata (PI 393567), was induced to flower and set seed when grafted to a rootstock of G. max. Ungrafted PI 393567 was previously unable to flower or produce seed under any tested environmental conditions.
The objective of our study was to characterize the flowering response, under noninductive long days, of scions from grafted combinations of a series of early- to late-flowering soybean isolines with different combinations of alleles at the E loci.
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MATERIALS AND METHODS
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Indeterminate soybean isolines of ‘Harosoy’ (Weiss and Stevenson, 1955) and ‘Clark’ (Johnson, 1958) were used in this study (Table 1) which exhibit a range of flowering times under most conditions. Seed of most isolines were kindly provided by Dr. Randall Nelson, Curator of the USDA Soybean Germplasm Collection and Dr. Richard Bernard, Univ. of Illinois. ‘OT94-47’ was developed at Ottawa by Dr. Harvey Voldeng, and the isolines with an L prefix were developed by Bernard et al. (1991). The experiment was done in a greenhouse where photoperiods were maintained at a minimum of 16 h using supplemental lighting from high pressure sodium lamps to extend natural daylength when necessary. Natural daylength at Ottawa, ON, has a maximum of 16.9 h including civil twilight or 15.7 h exclusive of twilight at the summer solstice. Temperature was maintained at 28°C during the day and 24°C at night. Seeds were germinated in vermiculite. After cotyledon emergence, seedlings were transplanted into 13-cm pots containing a sterilized soil mix in a ratio of 3:2:1:2:2 of loam, peat moss, sand, vermiculite, and crushed brick, respectively. These plants were used as rootstock material. Additional seeds of each isoline were planted in vermiculite 1 wk after the rootstock had the first expanded trifoliolate leaf. This second planting was used as a source of scions.
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Table 1. Genotypes of soybean isolines used in grafting studies. In the table, e represents recessive, early-flowering alleles while E represents dominant, late-flowering alleles.
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The rootstock was prepared for grafting by cutting the main stem between the first and second trifoliolate leaves. A longitudinal cut was made in the stem to provide a place to secure the scion. All but one axillary bud on the rootstock were removed to encourage growth of the scion. The single axillary rootstock bud was allowed to grow in conjunction with the scion to allow interaction between the two genotypes. Seedlings with unopened cotyledons were selected for scions and the root was removed. The hypocotyl was cut into a wedge shape below the cotyledons and then inserted into the cut in the main stem of the rootstock. The point of attachment between the scion and rootstock were wrapped with Parafilm laboratory film (American National Can, Menasha, WI). The entire plant was then covered with a perforated plastic bag to maintain humidity. The bag remained over the plant until the scion began growing (
1 wk). Flowering was defined as first appearance of conspicuous flower petals at any node on the scion and flowering date was recorded. Days from planting to flowering was calculated for each scion.
The first Harosoy isoline experiment using six isolines (OT94-47, Harosoy, ‘L64-4584’, ‘L67-2324’, ‘L71L-3004’) was replicated twice in time with the first replication rootstocks planted on 20 June 2000 and the second replication planted on 1 Feb. 2001. Within the first replication, there were six plants with each graft combination, and within the second replication there were four plants with each graft combination. The number of plants were reduced in the second replication due to the low amount of plant-to-plant variation. Ungrafted and self-grafted controls were also grown. Scions in this experiment received one of two treatments during the experiment; foliated, where the scion was allowed to grow normally, and defoliated, where leaves were removed from the scion before they had fully expanded. As plants grew older, scion leaves became smaller and it become more difficult to determine when they were nearly fully expanded. In this case, leaves were removed when the next developing leaf had leaflets which were not touching according to the Fehr and Caviness (1977) node counting system.
A second experiment was conducted to determine if the background of the isolines used in grafting experiments would influence the time to flowering. Early isolines, OT94-47 and L92-21, and late isolines, L71L-3004 and L65-3366, of Harosoy and Clark, respectively, were used in reciprocal grafts (see Table 1 for genotype of isolines). The planting and grafting procedures were identical to those used previously. Treatments were replicated twice in time with six plants in the first replication and three plants in the second replication. The first replication rootstocks were planted 10 Oct. 2000 and the second on 7 Feb. 2001. This experiment was done with foliated scions only. Ungrafted plants were grown as controls.
A third experiment was conducted with cultivars that were later maturing than the latest isoline. Seed of two cultivars from each of Maturity Group (MG) VI (‘Boggs’, ‘NC Roy’), MG VII (‘Benning’, ‘Santee’), and MG VIII (‘Kuell’, ‘Prichard’) was kindly provided by Dr. Randall Nelson, Curator of the USDA Soybean Germplasm Collection. The planting and grafting procedures were identical to those used previously. Three to four plants were used for each graft combination. The rootstocks were planted 15 and 22 Nov. 2001. This experiment was performed with foliated scions only. Ungrafted plants were grown as controls.
Each grafting combination or ungrafted genotype was analyzed as a fixed effect. An ANOVA was done on all data using the General Linear Model procedure of SAS (Cary, NC) and, where appropriate, a protected LSD (P = 0.05) was used to determine differences in scion days to first flower among graft combinations or ungrafted genotypes.
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RESULTS
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The series of isolines used in this work have late-flowering alleles at between zero to five flowering-time loci in a common genetic background (Table 1). Time to flowering for ungrafted controls ranged from 22 d for OT94-47 to 83 d for L71L-3004 under long (16-h) photoperiods (Table 2). For the nondefoliated plants, there were no significant flowering time differences between ungrafted and self-grafted control plants (Table 2). The grafting process was highly successful (data not shown). Scions showed vigorous growth within 1 wk of grafting and continued to grow normally through the duration of the experiment.
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Table 2. Days to flower of scions from grafts between soybean photoperiod-sensitivity isolines with different combinations of maturity genes under  16-h daylength in a greenhouse.
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Graft combinations of isolines allowed us to test flowering time interactions between genotypes. Late-flowering rootstocks did not delay flowering of OT94-47 (the earliest flowering isoline) scions compared with self-grafted OT94-47. OT94-47 scions flowered in 27 d regardless of the rootstock (Table 2). Flowering of the three intermediate isolines (Harosoy, L64-4584, L67-2324) was delayed on average 8.9 d by rootstocks of L71L-3004, the latest-flowering isoline. Results were similar for defoliated scions although the delaying effect of L71L-3004 rootstocks was larger, 25.2 d on average, on the three defoliated intermediate isolines (Table 3).
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Table 3. Soybean scion flowering time differences between graft combinations and the respective self-grafts. Positive values indicate that the rootstock promoted flowering of the scion. Negative values indicate that the rootstock delayed flowering of the scion.
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Early-flowering rootstocks generally promoted flowering of scions. Scions grafted to OT94-47 rootstocks flowered in 30 d regardless of the genotype of the scion (Table 2). Flowering of L71L-3004 scions was promoted in every graft combination (Table 3). This promotion effect was largest when L71L-3004 was grafted to OT94-47, which caused the L71L-3004 scion to flower 54 d earlier compared with the L71L-3004 self-graft. The response of the L71L-3004 scion was correspondingly smaller as late-flowering alleles were added in the rootstock. Similar results were obtained when scions were defoliated except the defoliated L71L-3004 scion flowered earlier when grafted to the three intermediate isolines (Table 2).
When self-grafted scions were defoliated, two of five isolines had significantly different flowering times compared with their respective nondefoliated self-graft. There was no pattern, however, since one defoliated self-graft flowered earlier (L67-2324) and one later (L71L-3004) than the respective nondefoliated self-graft control. When grafted defoliated scions were compared with their corresponding nondefoliated graft combinations, several significant differences were observed; however, to examine the effect of rootstocks on defoliated scions, we compared defoliated scions to their respective defoliated self-graft. In this comparison, only two combinations were significantly different and defoliation of L71L-3004 scions resulted in earlier flowering in graft combinations with Harosoy and L64-4584 rootstocks compared with defoliated L71L-3004 self grafts.
To confirm that floral promotion of early-flowering rootstocks was not specific to the Harosoy background of the isolines used in this study, we made graft combinations between early and late-flowering isolines both within and across two genetic backgrounds. The cultivar Clark has also been used in backcrossing programs to incorporate combinations of flowering-time alleles, and corresponding Clark and Harosoy isolines were used (Table 1). Early flowering resulted from all combinations of early- and late-flowering graft combinations both within and across genetic backgrounds (Table 4). Since we were limited to maturity group V in the isoline series, we used several even later-maturing cultivars to make graft combinations with OT94-47 (Table 5). Flowering of OT94-47 was not delayed by grafting to rootstocks of any of the maturity group VI to VIII cultivars. All of these late-maturing cultivars flowered early on OT94-47 rootstocks.
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Table 4. Days to flowering of scions from grafts between early- and late-flowering ‘Harosoy’ and ‘Clark’ soybean isolines under 16-h daylength in a greenhouse.
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Table 5. Days to flowering of late flowering cultivars, and scions from grafts between an early-flowering ‘Harosoy’ isoline (OT94-47) and late-flowering soybean cultivars under 16-h daylength in a greenhouse.
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DISCUSSION
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The soybean photoperiod-sensitivity genes studied (E1, E2, E3, E4, E7) function to detect and delay flowering under noninductive photoperiods. Differences between late- and early-flowering alleles at these loci become apparent under longer noninductive photoperiods (Cober et al., 2001). The term noninductive could more correctly be called less-inductive since late-flowering genotypes do eventually flower in non-inductive photoperiods. All genotypes flower similarly and early under inductive short photoperiods (Cober et al., 1996; 2001; Cober and Voldeng, 2001). These flowering-time loci were identified using classical genetic procedures and in all cases F2 populations segregating at a single locus fit the ratio of 3 late flowering: 1 early flowering plant (Bernard, 1971; Buzzell, 1971; Buzzell and Voldeng, 1980; Cober and Voldeng, 2001). Late flowering was dominant or partly dominant over early flowering. Following these two lines of evidence (photoperiod response and genetic studies), we hypothesized that floral inhibition would play a dominant role in graft combinations of early- and late-flowering isolines. While there were reports in the literature of graft combinations promoting flowering, none of these studies used near-isogenic lines which minimize the effects of genetic background.
Our working hypothesis, based on photoperiod response experiments, was that early flowering was the ground state in soybean and that inhibitors delayed flowering under noninductive conditions. This is similar to the model of Simpson et al. (1999) for Arabidopsis where they concluded that flowering is normally actively repressed in Arabidopsis. Of the 10 early-scion and late-rootstock combinations, three scions were delayed while seven scions were not significantly affected. With the reciprocal 10 late-scion-early-rootstock combinations, eight scions were promoted while one was not significantly affected. Clearly, floral promotion played an important role in many graft combinations contrary to our working hypothesis. Floral inhibition seemed to play a less important role than floral promotion. Evidence for this is seen in two ways. First, the higher number of floral-promoting graft combinations (eight) as compared with the number of flower-delaying graft combinations (three). Second, when the three flower-delaying combinations were compared with their reciprocal grafts, the mean flower delay (8.9 d) is smaller compared with the mean flower promotion (17.9 d).
The lack of a flowering delay of OT94-47 and L92-21 scions grafted to late-flowering lines may be interpreted as a lack of inhibitor receptors in these early-flowering lines. OT94-47, however, has exhibited a photoperiod response at 20 h (Cober et al., 2001) and under low red:far-red light quality 20-h photoperiod (Cober and Voldeng, 2001). In addition, L92-21 contains late-flowering alleles at the E7 locus. This would preclude the explanation that a lack of inhibitor receptors allows early flowering in L92-21 if these flowering-time genes indeed function as receptors for floral inhibitors. An alternate hypothesis for the lack of flowering delay of OT94-47 and L92-21 grafted to late-flowering lines may be that some floral inhibitors are not graft-transmissible. In pea, fun1, now know as phyA (Weller et al., 2001), rootstocks were able to delay flowering of grafted scions (Weller et al., 1997); however, work with phyB showed that the floral inhibitor was not graft-transmissible (Weller et al., 2001). Perhaps some of the late-flowering soybean loci are similar in action to phyB in pea.
The defoliation treatment provided an opportunity to observe the effect of scion leaves on flowering time. Leaf-produced floral inhibitors played a role in controlling flowering time. Evidence of this was the earlier flowering of defoliated L71L-3004 scions grafted to earlier-flowering rootstocks compared with the same graft combination where the scions retained their leaves. Leaves are a source of floral inhibitors for a number of species (cocklebur, Withrow and Withrow, 1943; black henbane, Lang and Melchers, 1943; mango, Kulkarni, 1986; pea, Murfet, 1971, Weller et al., 1997; and strawberry, Thompson and Guttridge, 1960). Leaves also seemed to be a source of floral promoters because three earlier-flowering isolines were delayed more when their scions were defoliated in grafts to the latest-flowering isoline.
Although our hypothesis was based on a dominant role for floral inhibitors, we found that floral promoters also played an important role in controlling flowering time in this study. All scions grafted to the early-flowering OT94-47 or L92-21 rootstocks flowered in 30 d (Tables 2, 4, and 5). Similarly, OT94-47 and L92-21 scions flowered in 27 to 30 d regardless of the rootstock to which they were grafted. Since OT94-47 scions grafted to later-flowering rootstocks flowered early regardless of the defoliation treatment, floral promoters must not originate only in mature leaves but might be produced in young leaves or flower buds. Our working hypothesis that early flowering was the ground state in soybean and that inhibitors delayed flowering only under noninductive conditions must be discarded since we see strong evidence of floral promotion overcoming floral inhibition even in combinations with the late-flowering isoline. Grafting of late-flowering scions to early-flowering rootstocks has been previously reported as a method of inducing flowering in late-flowering lines in field crossing blocks in short-season areas (Beaver and Nelson, 1981).
In this analysis of soybean isolines, flowering time ranged from 22 d in an isoline with no known late-flowering alleles to 83 d in an isoline with late-flowering alleles at five loci. None of these genes have been characterized at the molecular level and no functions are known for these genes. It is likely that as developments in molecular biology continue, soybean will follow the pea model where classical photoperiod genes are now described by their gene product (fun1 = phyA, Weller et al., 1997; lv = phyB, Weller et al., 2001). Using the terminology of Reeves and Coupland (2001), we assume that soybean E loci function in the photoperiod-sensitivity pathway (homologous to the long-day pathway of Arabidopsis).
In conclusion, it appears that both floral inhibitors and promoters are active in determining flowering time for soybean under noninductive conditions. Under noninductive conditions, early flowering in soybean results from a combination of a lack of floral inhibitors plus the action of floral promoters. Our results indicate that both floral inhibitors and promoters are produced in leaves, developing leaves, or buds. Promoters and inhibitors mediate flowering time simultaneously and antagonistically.
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NOTES
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ECORC Contribution no. 02-99.
Received for publication June 13, 2002.
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ABSTRACT
INTRODUCTION
