The interplay between ovule number, pollination and resources as determinants of seed set in a modular plant.

Marina M. Strelin,Marcelo A. Aizen

doi:10.7717/peerj.5384

Abstract

BackgroundA classical dichotomous perspective proposes that either pollination or plant resources limit seed production. However, ovule number could also be limiting when pollination results in complete ovule fertilization and there are more plant resources available than needed to develop seeds. Moreover, this dichotomous view assumes that all flowers of a plant have equal access to a shared pool of resources, although these are frequently compartmentalized within plant modules, for example, inflorescences. How ovule number, pollination and resources affect seed production in physiologically-compartmentalized rather than physiologically-integrated plants has yet to be explored. We used raspberry (Rubus idaeus) to address this question.MethodsWe first assessed if ovule number affected the fraction of ovules that develop into seed (i.e., seed set) and whether this effect related to the extent of physiological integration among flowers within plants. This was achieved by statistically testing predictions on the sign and level of plant organization (i.e., among flowers within inflorescences, among inflorescences within ramets, and among ramets) of the relation between ovule number and seed set given different degrees of physiological integration. We then explored whether the relation between ovule number and seed set was affected by plant age (used here as a surrogate of resource availability) and pollination intensity (open-pollination vs. exclusion).ResultsWithin inflorescences, flowers with more ovules set a larger fraction of seeds. On the other hand, seed set at the inflorescence level was negatively related to the average number of ovules per flower. Seed set increased with ovule number and open-pollination, and decreased with ramet age. However, ovule number explained more variation in seed set than ramet age and pollination treatment. Ramet age affected the strength of the relation of seed set to ovule number, which was stronger in old than young ramets. Pollination did not alter the strength of this relation to any significant extent.DiscussionResults reveal the importance of ovule number as an overriding factor affecting seed set. Within inflorescences, resources appear to be differentially allocated to developing fruits from flowers with many ovules. This is consistent with the fact that in the raspberry a large proportion of the carbon invested in fruit development is fixed by the inflorescence subtending leaf. Differential resource allocation to flowers with many ovules is not affected by pollinator exclusion, being stronger in resource-exhausted ramets. This suggests that the effects of pollen limitation and resource allocation are compartmentalized at the inflorescence level. Consequently, modular plants can be viewed as reproductive mosaics where either ovule number, pollination or resources limit the number of seeds set by different flowers, so that improvements in any of them could increase plant seed production.

Highlights

Seed production can be affected by a diversity of factors acting during flower and fruit development (Primack, 1987)
We propose that: (1) ovule number has a density-dependent effect on flower seed set, with the sign of this effect and the level at which it originates depending on the extent of physiological integration among flowers at these different levels (Fig. 1); (2) resource limitation at the whole plant level increases within-plant variation in flower seed set, thereby strengthening the dependence of seed set on ovule number; and (3) a density-dependent effect of ovule number on flower seed set can persist despite some flowers being pollen-limited, as long as the flowers are not physiologically integrated at the whole plant level
A mosaic of reproductive limits Considering that all the study factors play a role in limiting seed set in raspberry, we propose that seed production in modular plants can be frequently subject to a mosaic of reproductive limits, with flowers in some modules limited by pollen, others by resources, and others by ovule number

Summary

Introduction

Seed production can be affected by a diversity of factors acting during flower and fruit development (Primack, 1987). In addition to not considering the contribution of ovule number to seed production, the classical dichotomous perspective on the limits of seed production assumes implicitly or explicitly that resources can move freely within the plant, with all flowers having equal access to resources (Wesselingh, 2007) Challenging this assumption, resource compartmentalization within plant morphological and physiological modules (e.g., inflorescences; Watson & Casper, 1984) has been shown as an important factor determining patterns of reproductive investment into flowers, fruits, and seeds (Guitian, 1994; Ida, Harder & Kudo, 2013, 2015; Dai et al, 2018). This suggests that the effects of pollen limitation and resource allocation are compartmentalized at the inflorescence level

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