Growth, architecture and reproduction
In Perilla, the effect of photoperiod on architecture is important because of the constraints that architecture places on reproduction. Architecture limits meristem number and, in this species, meristem number is a resource essential for flower production. This experiment has demonstrated that photoperiod affects architecture simply by determining flowering time: plant growth curves did not differ between day-length treatments until the southern-treatment plants began to flower ( Fig. 2). At flowering, apical meristems were converted into inflorescences, which precluded further vegetative development and thereby fixed plant architecture.
Because the southern-treatment plants flowered earlier, they had fewer branch apices available for flowering than the plants in the northern treatment ( Fig. 2d). Consequently, architectural constraints were more strongly limiting for the southern-treatment plants. Despite limitations on inflorescence number, these plants suffered only a moderate (approximately 14%) reduction in seed number compared with the northern-treatment plants, and total seed mass did not differ between treatments ( Fig. 4d,f). Plasticity at the level of the inflorescence allowed southern-treatment plants to compensate for fewer inflorescences by increasing the number of flowers and seeds produced per inflorescence ( Fig. 3 and Fig. 4b).
Although seed production is theoretically not limited in either treatment (given indeterminate inflorescences), total seed number per plant actually remained within a fairly narrow range ( Fig. 4d), indicating that seed production was in fact limited by one or more resources. Plants in both treatments made a similar total number of seeds, and therefore the number of seeds per inflorescence was somehow less limited in the southern-treatment plants. One possible explanation is that mineral nutrients set the upper limit on seed production. Plants in both treatments presumably had equal access to nutrients because they had the same root mass (t-test, P = 0.98) and received the same amount of fertilizer every week. If mineral nutrients limited seed production, then perhaps all the plants were able to produce roughly the same mass of seeds ( Fig. 4d,f) and the southern-treatment plants simply packaged them into fewer but larger inflorescences ( Fig. 3).
If, instead, carbon limited seed production, then a higher photosynthetic rate might explain how southern-treatment plants can support more seeds per node (and thus per leaf) than the northern-treatment plants. Because the southern-treatment plants flowered nearly 3 weeks earlier than the northern-treatment plants, the leaves present during seed fill were, on average, younger. In Perilla, photosynthetic rate reaches its peak at full leaf expansion and declines steadily with leaf age ( Batt & Woolhouse 1975), and the leaves on the southern-treatment plants were therefore probably capable of assimilating more carbon during seed fill than leaves in the later-flowering group.
Another mechanism by which plants can enhance total carbon gain is by retaining actively photosynthetic leaves for a longer time. Some evidence for this was found among southern-treatment plants. Although leaf drop in this treatment occurred 3 weeks earlier than in the northern treatment, it began at the same whole-plant developmental stage (late in seed development) ( Fig. 5). Thus, in Perilla, leaf loss is not simply a function of leaf age but instead appears to be triggered by seed maturation, as in soybean ( Noodén 1984). Moreover, senescence proceeded more slowly in southern-treatment plants. The mechanism behind the treatment difference in senescence rate is not clear, but it may have allowed southern-treatment plants access to relatively more carbon to support seed fill.
Just as the distribution of seeds among branches differed between day-length treatments, so did the distribution of carbohydrates. This result is consistent with other work showing that architecture influences carbohydrate translocation patterns ( Chapman et al. 1992 ; Botella et al. 1993 ). The stage at which plants were labelled and the location of the source leaf also significantly affected patterns of carbohydrate translocation, as in a previous greenhouse labelling experiment ( Preston 1998b).
Some of the translocation patterns were similar between the day-length treatments. For example, in both treatments, allocation to roots gradually tapered off throughout development ( Fig. 8). This pattern is consistent with the observation that flowering in Perilla is accompanied by a decline in root growth ( Woolhouse 1983). Both day-length treatments also showed a drop in stem activity between the first and second reproductive stages ( Fig. 8), which was similar to the pattern observed in the earlier labelling experiment ( Preston 1998b). In that experiment, plants harvested early (1 week after labelling) still showed high levels of stem activity, which suggested that assimilates were remobilized between labelling and the final harvest, perhaps to support seed fill.
The greatest difference between the treatments was in the activity per seed at labelled nodes ( Fig. 6). In plants labelled at the vegetative stage, activity per seed was significantly higher in the northern- than the southern-treatment plants, and activity per seed was negatively associated with seed number. In plants labelled at the second reproductive stage, this pattern was reversed. These contrasting patterns may be explained by a difference between labelling treatments in the origin of the labelled assimilates (i.e. current vs. remobilized) allocated to seeds. Plants labelled while vegetative had not even begun to flower when they were labelled, and therefore any activity recovered in seeds must have been remobilized from elsewhere in the plant. In contrast, plants labelled at the second reproductive stage were maturing seeds at the same time that they took in labelled carbon, thus developing seeds had access to labelled current assimilate.
In the plants labelled while vegetative, assimilate was remobilized and then distributed among seeds developing at the labelled node. There were fewer seeds per node in the northern- than in the southern-treatment plants (significant for node 6, t-test, P = 0.0006), suggesting that the activity per seed was greater under the northern treatment because these plants had fewer seeds over which to spread a similar amount of remobilized carbon. In plants labelled during the second reproductive stage, seeds were importing carbon at the time plants were labelled, and results from these plants are consistent with conventional expectations that current assimilates flow from a source leaf into the nearest ( Wardlaw 1990) most active sink ( Wardlaw 1990; Minchin et al. 1993 ) that has a direct vascular connection to the source leaf ( Watson & Casper 1984; Wardlaw 1990). For example, seeds at the labelled node maintained their priority over seeds at more distant nodes ( Fig. 6) and seeds in other orthostichies ( Fig. 9). Furthermore, the amount of activity translocated to each seed at the labelled node increased between the first reproductive stage and the second, when the demand for carbon at the labelled node was greatest. This was most dramatic in the southern-treatment plants labelled at leaf 6, where the activity of seeds at the labelled node increased not only in absolute terms ( Fig. 6) but also relative to other seeds developing in the labelled orthostichy ( Fig. 7).
The size of the increase in activity per seed between the first and second reproductive stages appeared to be related to the number of seeds maturing on each inflorescence. The southern-treatment plants, which made more seeds per inflorescence than the northern-treatment plants, showed the more dramatic increase between reproductive stages. This pattern was echoed within the northern day-length treatment: the greatest increase in activity per seed occurred at node 9, the node with the most flowers per inflorescence. It is important to note that activity per seed increased, not just total activity of all seeds at a node, because it suggests that the number of seeds produced at a node influenced the amount of labelled assimilate available to each seed at that node.
These results show clearly that differences between the day-length treatments in morphology and reproduction were correlated with differences in carbon allocation, but factors other than assimilate demand may also have influenced the observed patterns. In addition to the activity of tissues that import assimilate (‘sinks’), such patterns typically depend on the amount of assimilate supplied by the source leaf and on the conducting tissue between them ( Minchin & Thorpe 1993; Minchin et al. 1993 ). The plants in the two day-length treatments differed in all three of these features. First, of the two treatment groups, southern-treatment plants made more seeds per inflorescence, which suggests that the assimilate demand at each node was also greater. Secondly, the southern-treatment plants had, on average, younger leaves at flowering and thus a potentially greater supply of assimilate at each source leaf than the northern-treatment plants. Finally, it is possible that the plants differed in vascular capacity as well. In Perilla, phloem development is inhibited at flowering and sieve tubes become partially blocked by callose ( Woolhouse 1983). As the northern-treatment plants had more time to develop phloem, they may have had more functional phloem cells during seed fill than the southern-treatment plants. It is therefore probable that variation in each of these components contributed to treatment differences in translocation patterns.
Nevertheless, the results from this experiment point to a prominent role for sink demand in carbon movement, whereas the roles of pathway and source appear to be less important. For example, differences in phloem capacity should have been manifest by the first reproductive stage, but translocation patterns were most similar at this stage. Furthermore, at every whole-plant developmental stage, the average age of leaves on the southern-treatment plants was less than the average for the northern-treatment plants, yet activity in the southern-treatment seeds was higher only during the second reproductive stage. In contrast, variation in the carbon demand of seeds, stems and roots over development was accompanied by parallel shifts in the distribution of activity among these tissues. Therefore, the interpretation of the data focuses on differences in patterns of seed production between the two treatments, even though carbon demand was only one factor influencing translocation patterns.
Ecological consequences of architecture
In this experiment, the photoperiodic environment strongly affected plant architecture, which in turn affected both the distribution and packaging of seed production and the allocation of carbon within the plant body. Whereas architectural effects on reproduction are obviously important to plant fitness, the ecological significance of the observed translocation patterns are not as clear. In a previous labelling experiment ( Preston 1998b), leaves varied in the amount of assimilate they supplied to branches at other nodes. In those plants, the consequences of leaf loss for the carbon budget of the rest of the plant would depend on the particular export patterns of the lost leaf. In this experiment, the day-length treatments did not differ in the absolute amount of assimilate that was exported beyond the labelled node (P = 0.95). Rather, they differed only in the amount of assimilate exported to other nodes relative to the amount retained at the labelled node. Thus, it is not clear that damage to a given leaf would have a differential effect on the whole-plant carbon economies of northern- and southern-treatment plants. It seems more likely that the distribution of seeds among branches would be ecologically important. For example, losing a source leaf to disease or herbivory would remove the primary source for a greater proportion of the seeds from a southern- than a northern-treatment plant.
In contrast, the relationship between architecture and reproduction obviously had potential fitness effects. Under some conditions, plants are able to overcome architectural constraints on reproduction, as was observed in this experiment. Compensation is not always possible, however. For example, there was no evidence that southern-grown plants in a garden experiment ( Preston 1998a) produced a greater number of flowers per inflorescence than the northern-grown plants. Together, these two experiments demonstrate that environmental effects on a whole-plant trait (architecture) can impose a constraint on another trait (inflorescence number). Under the right conditions, however, plasticity at other morphological levels (flowers per inflorescence and seeds per flower) can compensate for this constraint.