Maternal Effects in Plants Author(s): Deborah A. Roach and Renata D. Wulff Source: Annual Review of Ecology and Systematics, Vol. 18 (1987), pp. 209-235 Published by: Annual Reviews Stable URL: http://www.jstor.org/stable/2097131 Accessed: 29/05/2009 08:31 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=annrevs. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact support@jstor.org. Annual Reviews is collaborating with JSTOR to digitize, preserve and extend access to Annual Review of Ecology and Systematics. http://www.jstor.org Anti. Rev. Ecol. Svst. 1987. 18:209-35 Copyright ? 1987 bY AnnuiiialReviews Inc. All rights reserved MATERNAL EFFECTS IN PLANTS Deborah A. Roach Departmentof Zoology, Duke University, Durham, North Carolina 27706 Renata D. Wulif Escuela de Biologia, UniversidadCentral de Venezuela, Apartado47114, Caracas, Venezuela INTRODUCTION Maternaleffects in plants were recognized as long ago as 1909 (32). Recent evidence, primarilyover the last 15-20 years, shows that maternaleffects can contributesubstantiallyto the phenotype of an individual, and as we show, this has importantconsequences for the interpretationand design of both ecological and genetic studies. Following a discussion of the consequencesof maternaleffects and an analysis of the different ways these effects can be estimated, we review the evidence for maternaleffects from the fields of physiological ecology, crop science, and quantitativegenetics. We do not review all of the literaturebecause that would be a monumentaltask; rather, we focus on representative studies from each of these fields. It is our contention that despite evidence that maternaleffects can have a large influence on offspring phenotype, few detailed studies have identified the specific causes of maternaleffects, particularlyin naturalpopulations. MATERNAL EFFECTS:DEFINITIONSAND CAUSES Variation in an individual's phenotype may be determinednot only by the genotype and environmentof that individualbut also by maternaleffects, i.e. the contribution of the maternal parent to the phenotype of its offspring beyond the equal chromosomalcontributionexpected from each parent. We distinguish three different classes of maternaleffects: cytoplasmic genetic, 209 0066-4162/87/1120-0209$02.00 ROACH& WULFF 210 endospermnuclear, and maternalphenotypic(Figure 1). Cytoplasmicgenetic maternaleffects are derived from the fact that organelles such as plastids and mitochondria can be directly transferredfrom the maternal plant to the offspring during ovule formation and development, and this transmissionis independentof nucleargenes. Molecularand quantitativegenetic studies have shown that cytoplasmic factors contributeto heritablevariationin both qualitative and quantitativetraits in plants. Discussions of cytoplasmic maternal effects in this paperare limited to identifyingthe generalphenomenonand do not focus on the details of transmission,which have been reviewed elsewhere (63, 164). A second class of maternaleffects in plants originates via the endosperm (Figure 1). During angiosperm development, multiple fertilization usually results in 3N endospermwith two nuclei from the maternaland only one from the paternalparent. Although the endospermis not always triploid, with the single exception of the Onagraceae,it always containsmore doses of maternal than paternal genes (177). The endosperm contains enzymes importantfor germination (72) and is also the source of nutrients for the developing embryo. As a consequence of the differential dosage of male and female genes, the female parentmay have a more importantrole in determiningthe characteristicsof this nutrientsource. A thirdclass of maternaleffects is phenotypic, resultingfrom the environment or genotype of the maternalparent. These influences may occur via structureor physiology (Figure 1). The tissues immediately surroundingthe developing embryo and endosperm are all maternal. These tissues, the integuments of the ovule and the wall of the ovary, eventually form the seed coat, fruit, and accessory seed structuressuch as the hairs, awns, and barbs. Such structuresare importantdeterminantsof seed dormancy, dispersal, and MATERNAL GENERATION OFFSPRING GENERATION I CYTOPLASMIC DNA EONMEV R NUCLEAR GENOTYPE DIRECTTRANSMISSION CYTOPLASMIC DNA ENVIRONMENTi PHYSIOLOGY - MATERNAL HENOTYPE ENDOSPERM NUCLEAR DOSAGE I STRUCTURE I I OFFSPRING 1FPHENOTYPE I NUCLEAR GENOTYPE ENDOSPERM NUCLEAR DOSAGE Figure 1 Path diagram showing maternal effects and other influences on the phenotype during the ofitspring generation. Solid arrows represent nmaternaleffects. I MATERNAL EFFECTSIN PLANTS 211 germinationtraits, and variationin these traitscan carryover to influence the mature phenotype of an individual. CONSEQUENCESOF MATERNAL EFFECTS Selection Studies Maternaleffects are generallyconsidered'troublesome'sourcesof errorin the sense thatthey are non-Mendelianand reducethe precisionof genetic studies. In fact, the actual influence of maternaleffects on the response to selection will depend on the type of maternaleffect involved. Environmentalmaternal effects will increase the amount of environmentalnoise and thus slow the response to selection. The amountof genetic covariationbetween consecutive generations will be furtherreduced if environmentalmaternaleffects persist for several generations(3, 89) or if there are substantialinteractionsbetween maternaleffects and the environment(3, 150). Cytoplasmic or nucleargenetic maternaleffects will inflate the amountof genetic variance but may slow the response to selection if the trait is completely undermaternalcontrol. Naylor (120) constructeda model to compare the response to selection for a population in which fitness differentials in offspring are undercomplete maternalcontrolvs a populationwith no maternal effects and complete offspring genetic control of fitness. Both models reached similar equilibriawith stabilizing selection, but the maternalcontrol model showed a slower response. Variationin an offspring trait may also be under the dual control of both maternaland offspring genotype. The response to selection for such a trait will depend on the correlation between the different effects. If there is a negative correlationbetween maternaland offspringeffects, then the response to selection will be slowed (38, 170, 179). Despite the fact that many traits probablyare under dual control, the consequences of this are rarely considered in selection studies. The consequences of maternaleffects for the response to selection may be further complicated by the correlationbetween maternaland offspring environments.If there is a high positive correlationbetween successive environments, then maternaleffects will be advantageousto individual offspring, particularlyif offspring do better in an environmentresembling the parental environment (92). Ecological Studies Variation in seed, seedling, and adult traits caused by maternaleffects can have importantconsequences for the ecology of an individual. Seed size, for example, is a trait for which a large maternaleffect has been demonstrated (see Evidence), and which has importantecological consequences. Studies 212 ROACH& WULFF have shown an effect of seed size on germinationcharacteristics(23, 34, 39, 182, 185), on seedling size (14, 136, 153, 184, 188), and on adult plant size and competitive ability (14, 39, 142, 154, 189). Variationin othermaternally derived traitscan similarlyresult in size hierarchiesand differentialfitness of individualswithin a population.Thus, our understandingand identificationof maternaleffects has importantconsequences for our understandingof plant distributionsboth within and between populations and communities. Maternal effects may complicate ecological studies, many of which are designed to identify the environmental factors determining the survival, reproduction,and distributionof individualspecies. In these studies, it may be difficult, if not impossible, to identify the environmentalfactorsdetermining success if the importantevents took place duringthe previous generation via maternaleffects. If maternaleffects do contributeto the traitsof interest, then a complete ecological understandingof the variation may require a multiple generation study and a separation of genetic and environmental maternaleffects. Maternaleffects may also complicate the interpretationof common garden studies. Phenotypicvariationamong plantsin a common gardenexperimentis generally attributedto genetic differentiation(24). Using tillers or cuttingsfor these types of studies can introducea bias from within generationcarry-over effects of the home environment(85). In a similar way, maternaleffects will result in maternalcarryovereffects if seeds are used in these experiments(7). The environment under which the seeds were matured, i.e. the maternal environment,may influence the growthof individualsin the common garden. In order to minimize this error, seed plants must be grown in a common gardenfor one (121) or several generations(7). However, persistentmaternal effects may still exist (3, 131). METHODS FOR ESTIMATINGMATERNAL EFFECTS Genetic Studies DIFFERENCES IN RECIPROCAL CROSSES The most direct quantitative evi- dence for unequal contributionby maternaland paternalparentsto the phenotype of offspring is throughreciprocalcrosses in which pairs of individuals serve as both maternaland paternalparent. A numberof differentreciprocal crossing designs may be used (for reviews see 26, 49, 106); the most common is the complete diallel. Reciprocalpairshave similarnucleargenetic contributions, and any difference in performanceof reciprocalpairs will be due to a maternal(or perhapsa paternal)effect. The relative importanceof maternal and paternaleffects can be determinedby comparingthe relative amountof variationbetween maternaland paternalhalf-sib families. Variancebetween family groups will be similar if there are no parentalinfluences beyond the MATERNAL EFFECTSIN PLANTS 213 equal chromosomal contributions, and maternaleffects will be indicated if there are greaterdifferences between maternalfamilies than paternalfamilies (106, 165). Paternaleffects have been found only in a few species (164). For dioecious plants, where it is not possible to use the same individual as both male and female parent,the best methodfor detectingnon-nucleareffects is a North Carolina Type-II design in which all possible matings are made between males and females (28, 106). RECIPROCAL SPECIFIC EFFECTS The next level of analysis partitionsmaternal effects into the portion due to differences between reciprocal crosses, which is consistent across all crosses sharing a similar maternalparent, and that which is due to the interaction between progeny genotype and the maternaleffect (73, 174). These interactioneffects have been termed 'reciprocal specific effects' and can be distinguished using the techniques of Hayman (73) or Cockerham& Weir (27). They are sometimes attributedto interactions between cytoplasmic maternal effects and offspring nuclear effects. Without furtherdetailed analysis, it is possible to argue they could also be due to an interactionof any other type of maternaleffect (Figure 1) with offspring nuclear effects. An even more detailed analysis of a diallel cross, which allows separation of additive and dominance components of reciprocaldifferences, has been worked out (41, 179), but to our knowledge this level of detail has rarelybeen appliedto studies in naturalpopulations(for an exception see 74). SEPARATING DIFFERENT TYPES OF MATERNAL EFFECTS It is important to be able to distinguish the different classes of maternaleffects because they have different evolutionary consequences. A number of experiments have attempted to distinguish cytoplasmic effects from other types of maternal effects by their persistence over generations (10, 21). The problem is that environmentaleffects may also persist for more than one generation (3). A more definitive identification of cytoplasmic maternaleffects can be made with specific crossing designs that repeatedlyuse the same maternallineage. For example, Corey et al (31) used a male tester in crosses with reciprocalF1 hybrids to show a cytoplasmic maternal effect for seedling size in Arabidopsis. Endosperm dosage maternal effects can be identified by their unequal contribution from male and female parent. Smith & Fitzsimmons (153) suggest that it is possible to identify an endospermeffect if one assumes that (a) at least two doses of factors are necessary to obtain, say, a heavy grain, and (b) a single dose has no effect on grain weight, and (c) the effect of three doses is equal to the effect of two doses. Their crossing scheme producedF1 hybridsbetween large- and small-seededparentallines of flax, and then F2's 214 ROACH& WULFF from permutationsof crosses among the Fl's. They reasoned that the mean weight of F2 grains should equal the averageof the parentallines if therewere endosperm dosage effects on grain weight. Their results did not show any dosage effects. Using a different technique, Millet & Pinthus (115) tested endospermgenetic maternaleffects on grainweight in Triticumaestivumfrom a comparisonof self and reciprocalcrosses of heavy- and light-seeded cultivars. They reasoned, that the mean weight of the F2 should equal the average of the grain weights of the two selfed lines. These techniques have not been applied elsewhere, nor have their assumptionsbeen tested. Phenotypic maternaleffects can be either genetic or environmental, and simple experimentaldesigns can be used to separatethese phenotypiceffects. The most common technique is to clone individuals over different environments prior to crossing (25). The relative contributionof genetics and environment to the offspring phenotype can then be evaluated. It is not possible to separategenetic and environmentalmaternaleffects in a single generation.However, an approximateseparationof these effects can be done with perennialspecies; this involves collecting seed over several years from the same maternalplant and calculating various covariances between seed weight and seedling size. Genetic and persistentenvironmentaleffects can then be separatedfrom transientenvironmentaleffects (98, 112). No study has ever considered all possible causes of maternal effects simultaneously.Thus, it is not possible to evaluate the relative importanceof the different origins of maternaleffects. Environmental Studies The general methodology used to study environmentalmaternaleffects is to place plants under different environmentalconditions and to observe traits expressed in the offspring generation.These studies measurean environmental carryovereffect and involve variablesof the environmentincluding light, nutrients,temperature,water, and growth substances. Most studies examine the effect of only one of these environmentalvariables at a time, except in studies done in naturalpopulations in which case the "environment"is not specifically identified. Environmentallyinduced genetic changes may occur as a result of these environmentaleffects (36, 42, 80), but these effects are rare and we do not include them in our definition of environmentalmaternal effects. Instead, we considerenvironmentaleffects as transientinfluencesthat endureone generationor, with diminishingeffect, into the second generation. It is often difficult to separateenvironmentaleffects acting directly on the seed from those acting on the mother and then the seed. In this paper, maternaleffects include all influences thattake place before seed dispersal. In other words, we include as maternaleffects all effects that occur afterembryo formation but before seed dispersal. MATERNAL EFFECTSIN PLANTS 215 EVIDENCE FOR MATERNAL EFFECTS Maternal Effects on the Seed SEED SIZE AND MINERAL COMPOSITION Genetic studies A large maternal effect on seed size, identified through differences between reciprocal crosses, has been found in Zea mays (43), Brassica campestris (150), Raphanus raphanistrum(110), and a numberof other species (180, reviewed by 2). Most of these studies unfortunatelyhave not separatedpossible sources of the maternaleffects, not even at the basic level of genetic versus environmentalcontributions.In one of the few studies that has separatedphenotypicmaternaleffects into genetic and environmental components, Antonovics & Schmitt (6) showed that both components had effects on propaguleweight in Anthoxanthumodoratum,but thatenvironmental maternaleffects predominated.In the only other genetic study of maternal effects with a noncultivated species in a natural population, Roach (135) showed reciprocaldifferences due to maternaleffects on seed size in Geranium carolinianum. Genetic studies with cultivatedplants have shown that maternalcytoplasm may directly influence seed size. For example, in crosses between small- and large-seeded flax varieties, Smith & Fitzsimmons (153) found reciprocal differences in seed weight. Curiously, parents producingsmall seeds had a largermaternaleffect than did those that producedlarge seeds. Persistenceof these differences into the F2 and F3 hybridsindicatedthatthe effects were due to maternalcytoplasm. In order to show cytoplasmic maternaleffects definitively, multiple generation studies such as this need to be done. Conclusions about the presence of cytoplasmic maternaleffects have sometimes been prematurelyreported in the literature. For example, Chandraratna& Sakni (21) showed a maternaleffect on grain weight in rice, and a model constructedby them assumedthatthis maternaleffect was due to cytoplasmic inheritance.However, the authorsacknowledge that later generationcrosses would be needed to show cytoplasmic inheritancedefinitively. Genetic studies of cultivated species have also demonstratedvarious types of maternaleffects on the mineral composition of seeds. Reciprocal differences, suggesting large maternaleffects, have been found for seed chemistry in pearl millet (16), seed oil in Lupinus (180), fatty acid content in maize (137), and protein content in dry beans (101) and soybeans (149), but not in Brassica campestris (150). In the case of dry beans, and in most cases with soybeans, these differences did not persist into the F2, suggesting that these are noncytoplasmic maternaleffects. Cytoplasmic maternaleffects may explain reciprocal differences in oil content in sunflowers, for it has been 216 ROACH& WULFF hypothesizedthat oil synthesis may occur primarilyin mitochondriaor chloroplasts (57). Unfortunately, a multiple-generationstudy was not done to confirm this conjecture. Environmental Studies Evidence for environmental phenotypic maternal effects may be inferredfrom studies in naturalpopulationsin which variation in seed size has been reported both among and within plant populations. Within populationsthe major source of variationis among individual plants (155, 162, 172); thus, either genetic or microenvironmentalfactors are an importantinfluence on the size of seeds produced.In these studies, variability in seed size has been correlatedwith environmentalfactors such as drought (144), temperature(113), and grazing (34). Studies in which single environmentalfactors have been examined, under controlledconditions, have shown that the effects on seed weight of maternal environmentalconditions depend on the timing of the treatment. Sionit & Kramer (151) found a decrease in seed weight in soybeans in response to water stress when the stress was appliedduringpod formationand filling, but no similar response occurred when the stress was applied at other stages of development. Decreased water availability for the mother plant results in decreased seed weight in a number of other species (114, 140, 183, 187), probably a result of decreased rates of photosynthesis and changes in seed maturationtime. Growth substancesappliedto the maternalplant may also affect seed size, particularlyif applied during the time of seed development and maturation. Hormonecontent in seeds varies duringdevelopmentand may have a regulatory role in directing the movement of assimilates toward the seed (12). Hormone content of seeds also varies with environmentalfactors; for example, the concentrationof abscisic acid is increased by water stress, decreased by low temperatures,and affected by the mineral nutrition of the parent plant (91). Moreover, seed weight correlates with endogenous ABA content (147). The role of hormones in seed development is poorly understood, and although several stages of seed growth and development are correlated with changes in hormone levels (46), these changes may not necessarily indicate differences in hormone action or be the cause of differences in rate of seed growth (64). Exposure of the parent plant to different temperaturesaffects the size of seeds producedin several species (3, 22, 47, 187). These effects have usually been ascribedto differences in assimilatesupply. However, since temperature affects both the rate of dry matteraccumulationin the seed and its period of development, maximum seed weight is not necessarily attained at the temperaturefavoring the highest accumulationof dry matter (173). Daylength MATERNALEFFECTSIN PLANTS 217 also affects seed weight, as for example in Chenopodiumrubrum(30). In this case, photoperiodictreatmentextremely early in development affected seed weight. In contrast, photoperiodiceffects on seed dormancy usually occur only at later stages of seed development (65). The effect of maternalresources on seed size has been studied by various methods. In many species, seed size increaseswith increasednutrientsupply (64, 125, 181, 187). In some cases, there is an interactionbetween maternal genetic and maternal environmental effects (105). In other species, seed weight remains stable despite increased nutrientsupply and increased plant growth (53). Similarly, in some species, partialshadingduringcertainstages of development may influence seed weight (88, 126), but in other species, shading may have no effect on final seed weight if the period of seed development is also increased (48). Environmentalfactors, such as grazing, may result in the removal of leaves, inflorescences, or seeds from the maternalplant. Studies have shown that partial defoliation of the maternal plant may lead to a decrease (107, 156) in mean seed weight, to no effect (100, 182), or to an increase(187). Sometimes a moreintensedefoliationmay increase ratherthan reduce mean seed weight (105). Leaf removal may affect carbohydrate supply and may also have major effects on hormonal and nutrient supply and on translocationpatterns. The removal of flowers or developing seeds has often been shown to increase seed size (48, 59, 108), most probably by removing reproductivesinks. While in many cultivatedspecies the seed concentrationof differentminerals is markedlyaffected by the external supply to the parentplant (117), in wild plants the elemental composition of seeds seems to remain relatively stable. In Senecio sylvaticus (167) and in Senecio vulgaris (53), seeds produced by plants grown in a range of nutrienttreatmentsmaintainedremarkably constantmineralnutrientconcentration;so did seeds of Grevillea leucopteris collected from plants grown in a wide variety of soil types (84). In Abutilon theophrasti, five minerals were tested; only nitrogen concentration showed a significantincreasein the seed in responseto an increasein parental nutrient status (125). These results suggest that, in species not artificially selected, seed quality may be relatively buffered against the variation in parentsupply. Given that nutrientsupply to the maternalplant may affect not only seed chemistry but also seed coat structureand hormone content (64), and given that nitrogen in seeds is stored mainly in the form of proteins, several of which may have a major role as defense against predators(118), more detailed studies are needed on the response of noncultivatedspecies to the nutrientsupply to the maternalplant. There is some evidence that nutrienttreatmentsapplied to the maternal plant can influence the nutritionalqualityof seeds, and thatgenotypes vary in 218 ROACH& WULFF response to this treatment.In a study of the effect of foliar urea sprays on grainproteinpercentageand grainyield, Altmanet al (4) found an increasein percentageprotein in the seed with increasednitrogenapplication.They also found a maternalgenotype by nitrogentreatmentinteraction,suggesting this type of maternaleffect has both a genetic and an environmentalcomponent. DORMANCY AND GERMINATION Genetic studies The primarycontrol of seed dormancyand germinationis through the maternal tissues surroundingthe embryo (109). In particular, control is via the seed coat (93) or other structuressuch as the lemma and palea (82). A maternaleffect on germinationmay also occur via an endosperm dosage effect (Figure 1), because the endosperm, which contains a larger maternal than paternal component, contains a number of enzymes importantfor germination (43, 72). Garbutt& Witcombe (60) showed, in Sinapis arvensis, that the seed coat (of maternalorigin) controls dormancy. The embryogenotype only affects dormancywhen there is a nondormantseed coat type. No study has ever addressedthe relative importanceof maternal tissues and endosperm to germinationpatterns. Genetic studies have shown a large maternaleffect on germinationpercentage in Zea mays (43) and Anthoxanthumodoratum (145). In studies with Dactylis (123) and Loliumperenne (76), maternaleffects found for germination percentage were due perhapsto cytoplasmic or cytoplasmic interaction effects, but in neithercase were multiple generationstudies done to confirm this. Reciprocal differences for seed longevity in soybeans are due to noncytoplasmicmaternaleffects, for the differencesdecreasedin latergenerations (96). In addition to influencing the rate or timing of germination, maternal effects can also influencethe sensitivity of seeds to environmentalconditions. In a study with Zea mays, a maternaleffect was found for sensitivity to cold during germination(17). Environmentalstudies Seeds of differentpopulationsor geographicalorigin have often been found to vary in germinationrequirementsand in degree of dormancy (11, 40, 113, 127, 129, 168). For example, in a study on Poa trivialis, Hilton et al (81) found that the germinationresponse to red/far-red ratios was relatedto the light quality to which the seeds were exposed during maturation in their natural habitats. Microclimate and site may also be importantdeterminantsof seed germinationpatterns. In a study of germination inhibition, in Chenopodium bonus-henricus, Dorne (40) showed that whereas the excised embryo was never dormant,germinationof intact seeds was dependent on seed coat thickness. The seed coat became thicker and MATERNAL EFFECTS IN PLANTS 219 containedmore polyphenols with increasingelevation, and this was reflected in reducedgermination.Moreover, plants transplantedto differentelevations showed a direct influence of the new environmenton seed coat inhibitionof germination.Common gardenexperimentssuggest that much of the variation in germination requirements among populations may be environmentally induced (40, 121, 127). But the importance of this to within-population variationin seed dormancyis not clear because few studies have been done in naturalpopulations (but see 87). The effects of specific environmentalconditions on seed germinationrequirementshave been recently reviewed (64-66). As a generalrule, the lower the temperatureduring seed development, the higher the levels of dormancy (130, 168) duringthe seed maturationperiod (139); this is also true if applied only during vegetative development (141). Generalizationsabout the effects of maternaltemperatureson seed germinationare difficult, however, because there may be considerable genetic variability in the response to maternal conditions. When clones of Plantago lanceolata were grown to maturityat two differentthermoperiods,the overall effect of higher maternaltemperature was a decrease in seed weight and an increase in the rate and percentageof germination.However, seed families differed in theirgerminationresponseto maternaltemperatures(as indicatedby significantinteractionsbetween family and maternaltreatment)as well as in the degree to which the response to germinationtemperaturedepends on the temperatureconditions during seed maturation(as indicatedby significantthree-wayinteractionsbetween family and germinationtemperatureand maternaltemperature(3). The existence of genetic variability in the response to maternaltemperatureswas also shown for pure lines of wild oats (138) and for different wheat genotypes (128). Daylength and light quality during seed development have been found to affect germination in several species (reviewed by 65, 66), and the photoperiodictreatmentshave been found to be most effective duringthe later stages of seed development. Light quality effects are most probablymediated by the phytochromesystem. For example, in Arabidopsisthaliana, exposure of plantsduringseed developmentto light with a low red/far-redratioresulted in seeds with low germinationpercentagein the dark, while exposureto light with a high red/far-redratio resulted in seeds with high dark germination percentage (62, 111). This suggests that the active form of phytochrome, induced by the light treatmentduring seed development, persists and acts in the dry seed. These effects are probably perceived by the developing seed itself. When developing buds are selectively illuminatedwith a fiber light, the receptorfor the red light stimulus is shown to be localized in the developing seed and not in the vegetative parts of the plant (62). Even in vitro cultured ovules are sensitive to red and far-redlight (163). Since light transmittedby chlorophyll-containingtissues will be enriched at the far-red end of the 220 ROACH & WULFF spectrum(152), seeds located in differentportionsof the inflorescenceor the canopy may be exposed to different red/far-redratios during development. The light-filtering propertiesof the maternaltissues surroundingthe seeds could be responsible for this light sensitivity. In an extensive study of many different species, Cresswell & Grime (35) found that the chlorophyllcontent of the investing structureswas negatively correlatedwith the capacityof seeds to germinate in the dark. The effects of maternalnutrientsupply and hormonelevel on dormancyand germinationhave been recently reviewed (64, 65). Although for many species, a positive correlation is found between increased nutrientsupply and germinationpercentage, an increase in nitrogen fertilizationcan result in an accumulation of germination inhibitors in the fruits (86). The effects of growth substancesvary accordingto the time of applicationand often interact with other environmentalfactors such as photoperiod(68). The interpretation of these effects is difficult because we know little aboutwhat fractionof these hormonesare translocatedfrom the motherplant, what fractionis synthesized in the seed itself, and how growthsubstancesare degradedduringseed drying (12). Many other environmentalfactors may affect seed germination. For example, exposure of the parentplants to drought stress during seed development decreased the duration of primarydormancy in wild oats (140), and growth of Plantago lanceolata under elevated atmospheric CO2 concentrationsincreasedgerminationpercentages( 186). In both studies however, considerablevariationoccurredin the responses among families, suggesting that genetic variability in the response of seed germination to maternal environmentalconditions may be widespread. Many of the environmentaleffects on seed dormancy could be due to changes in the structureor permeability of the seed coats. Photoperiodic treatmentshad a significant effect on the permeabilityof Ononis sicula seeds (67), and the addition of minerals and growth substanceshas been found to alter seed coat structurein several species (reviewed by 64). In a study with soybeans, Nooden et al (122) found that seed coat permeabilitywas increased by the addition of minerals and cytokinins. Since drought decreases the productionof cytokinins in the root and mineralflux to the shoot (5), water stress may induce the productionof more impermeableseeds. Variation in other accessory seed structureshas been less studied, but it is known that pappus length in Leontodon hispidus is altered by seasonal changes in the environment (58). Given the numerouseffects of maternalenvironmentalconditions on seed dormancy, it is not surprisingthat the timing of dispersal influences seed germinationrequirements.During the growing season, environmentalconditions change, and this is reflected by a change in the quality of offspring MATERNAL EFFECTSIN PLANTS 221 producedat different times (8, 136). In Frasera caroliniensis, for example, seeds that overwinteredon the parent plant requiredwarm stratificationin addition to the cold stratificationrequiredby seeds collected earlier in the season (9). As a result, in late maturingseeds, germinationwas spreadover several seasons. WITHIN-PLANTEFFECTS ON SEED SIZE, DORMANCY, AND GERMINATION Single plants may produce seeds differing in size and germinationrequirements. These effects range from the productionof clearly dimorphic seeds such as the aerial and subterraneanachenes in Emex spinosa (176), or the achenes produced by disk and ray flowers in many Compositae, to a continuous variationin seed size associated with position of a seed on a mother plant during development. Positional effects and their effects on seed structure and dormancyhave recently been reviewed (64, 65, 148). In the classic example of Aegilopsis ovata, Dattaet al (37) found thatthe grainsproducedin the upper portions of the spikelet were more dormantand weighed less than those producedin the lower portionsof the spikelet. Similareffects have been described for Rumex (19, 107, 108). More recent examples include the variabilityin structure,germinationrequirements,and dispersalability of ray and disk achenes in Heterotheca latipholia (171), the differences in size and germination requirements between aerial and subterraneanpropagules in Amphicarpea bractata (146), and the variability in size and dormancy of seeds producedat differentpositions in the umbel in Pastinaca sativa (79). It has been suggested that within-plantvariabilityin seed size may be affected by the timing of fertilizationor by the numberof competing ovules per fruit (110). Silvertown (148) has proposedthat the differentialrates of ripeningof the embryo and enveloping structures(somatic heterochrony)could account for many of the polymorphismsobserved within plants. As much as an eight-fold variationin seed weight was observed in single plants of Lomatiumgravi (162), almost a six-fold variability in Raphanus raphanistrum (155), and about a two-fold variation in Pastinaca sativa (79) and in Desmodium paniculatum (187). In the latter species, within-plant variability is affected by nutrientsupply. Seed size has often been found to vary with position on the plant or the infrutescence, as for example in Impatienscapensis (172), in wheat (132) and in many Umbelliferae(79), and with position in the fruit (155). This variationof seed weight with position in the pod is commonly found in legumes (142, 187) and is sometimes associated with variation in mineral content (83). In summary, within-plantvariationin seed size and dormancyemphasizes the sensitivity of these traits to environmentalvariation. Controlledenviron- 222 ROACH & WULFF ment studies have identifiedspecific environmentalfactorsthatinfluence seed size and dormancy,but the importanceof these specific environmentalfactors to variation in naturalpopulations is not clearly understood. Maternal Effects on Later Life Traits SEEDLINGS Genetic and environmental studies A large number of studies have been done with Lolium perenne, and the results showed that maternaleffects can have a substantialinfluence on an individual'sphenotypeat the early seedling stage, and thatthese effects diminishover time (10, 44, 76-78, 159, 161). Up to the thirdleaf stage, leaf number, leaf size, and tiller numberin L. perenne were predominantlyundermaternalcontrol. At the fifth leaf stage, maternal effects were not present, or they were combined with offspring genetic effects. Similar studies with Dactylis have shown maternaleffects for seedling growth rate, leaf area, and tiller number (123, 124). In these studies, cytoplasmic effects or interactionsbetween cytoplasmic and nuclear effects were suggested as the cause of these maternalinfluences. Cytoplasmicmaternaleffects on seedlings were identifiedin an experiment with Arabidopsis using male testersin crosses with reciprocalF, hybrids(31). Results indicatedlarge and persistentmaternaleffects for seedling root length and plant weight, suggesting that these effects were due to cytoplasmic influences. A number of studies have shown an indirect maternaleffect on seedling size via seed size (1, 98, 104, 143, 154, 188). A positive correlationbetween seed and seedling size is evidence for a maternaleffect in species for which seed size is under maternalcontrol. In a study with tobacco, Van Sanford& Matzinger (169) suggested that the stability of seedJing weight over several environmentswas consistent with an indirectmaternaleffect via seed size. In other words, because of the dependence of early seedling growth on the materials stored in the seed, maternal effects on the seed had a larger influence than the immediate environmentin determiningthe early juvenile phenotype. In a similar way, reciprocal differences in alfalfa for seedling height and forage yield were largely attributableto the correlationbetween seed size and the photosyntheticarea of seedlings (18). In studies such as these, it is not possible to distinguish between genetic and environmental maternaleffects because maternalgenotypes were not randomizedover environments. Although he could not completely deconfound genetic and environmentaleffects, using Phalaris tuberosa Latter (98) found that genetic and persistent environmental maternal effects on seed size subsequently influenced seedling weight and growth per tiller. Environmentalmaternal effects on seed size, on the other hand, influenced the time to emergence of MATERNAL EFFECTSIN PLANTS 223 leaves and tillers and also seedling tiller number. Latter suggested that qualitative differences may exist between genetic and environmentaleffects of seed size: Whereas the genetic maternaleffects might depend on differences in the levels of endogenous gibberellinsand auxins, the environmental maternaleffects may influence nutrientlevel and differences in embryo size (98). Maternaleffects may differ among even closely relatedspecies. In Lolium perenne, large genetic maternal effects were found for the rate of leaf appearance(44). In L. multiflorum,however, no maternaleffect was found for this trait despite a maternaleffect on leaf size (45). In the study with L. multiflorum,maternaleffects contributedto variationin thirdleaf size, due to additive genetic maternal effects on leaf length and maternal interaction effects on leaf width. The pattern of maternal effects in this species was similar to studies with other Lolium species in that maternal effects were found for early leaf size but were absent at the sixth leaf stage. Environmentalmaternaleffects may also have a significantinfluenceon the seedling phenotype. In Plantago lanceolata, exposure of the parentplant to different CO2 levels and temperatureregimes affected seedling sizes and growth rates. However, families differed in both the extent and the direction in which seedling developmentwas affected by maternaltreatments(3, 186). The relationship between maternaltreatmentsand seedling response is not always straightforward:In Senecio vulgaris the nutrient requirements of seedlings did not correlatewith the nutrientconditionsduringseed maturation or with the nutrientcontent of the seeds (54). There have been very few quantitativegenetic studies of maternaleffects for seedlings in naturalpopulations.A study with G. carolinianumshowed no evidence for maternaleffects on seedling traits(135). Similarly, therewere no maternaleffects beyond germinationin Anthoxanthumodoratum (145). In general, relativeto the numberof maternalenvironmentalstudiesdone at the seed stage, few have considered the influence of specific environmental factors during the maternal generation on seedling traits, particularly in noncultivated species. ADULTS Genetic and environmentalstudies Several studies showing reciprocaldifferences for yield components in cultivated plants have been reviewed by Aksel (2). Singh & Murty(150) also found reciprocaldifferences in Brassica campestris for a numberof yield charactersincluding length of the fruit and yield per row. In their study, differences between reciprocal crosses were influencedby the environment,suggestingthat some motherswere betterable to exploit favorableconditions. Maternaleffects have also been found for the probabilityof flowering and for the numberof inflorescences in L. perenne 224 ROACH & WULFF (74), and also for adultplantheight in Nicotiana rustica (89). In some studies, yield components show no maternaleffect (95). One of the best-known examples of maternalcytoplasmic inheritanceand its influence on adultcharactersis male sterility. Since this has been the object of numerousstudies and reviews (33, 69), and probablyrepresentsa distinct phenomenon, we do not consider it here. Maternaleffects on adult traits may be indirect via seed size effects (39, 175). For example, Stanton (154) found a positive correlationbetween seed size and adult reproductiveoutput in Raphanusraphanistrum.The influence of seed size on yield componentsmay dependon environmentalconditions. In a study with Austrianwinter field pea, Murrayet al (119) found thatthe yield of peas established from small-sized seed was significantly lower than the yield of peas from large- or medium-sized seed under cool, wet conditions. When the environmentalconditions were not adverse but ratherwere favorable for pea growth, there were no differences in yield associated with seed size. Maternaleffects on adultsmay also be indirectvia otherearliereffects. For example, in Lolium multiflorum,maternaleffects on adulttiller numberwere explained by the observation that earlier in the life cycle, tiller number is affected by maternalinfluences such as seed reserves and hormonaleffects. And, by the nature of the tillering process, maternallycaused early differences can carry over to the adult stage. Furthermore,since the number of inflorescences was related to the number of tillers, maternal effects on inflorescence numbermay also have been due to an earlier nutritionaleffect (45). An indirectmaternaleffect may also occur due to variationin seed chemical composition, produced by fertilization treatments. For example, in Phaseolus vulgaris nitrogen fertilization increased protein content and seed size, but smaller seeds with higher protein content producedhigher yielding plants than did the largerones (133). In noncultivatedspecies, seed composition seems to remain relatively stable; in Abutilon theophrasti, however, seeds that differed only in nitrogen content producedplants that differed in their competitive abilities (125). Studies with Loliumperenne have shown inconsistentresults even for the single trait-flowering time. Thomas (159) found that time of flowering was under genetic control of the individual and showed no maternal control between populations. However, Hayward (74) found both additive genetic controland a substantialmaternaleffect. Of the total variationin time, 20% of flowering in Hayward'sstudy was undermaternalcontrol. Furtherstudies by Hayward and colleagues (77, 78) using a within-populationdiallel analysis also showed a degree of maternalcontrol for time of flowering. However, in Lolium multiflorum,the only adult trait for which there were no reciprocal MATERNAL EFFECTSIN PLANTS 225 differences was flowering time (45). Flowering time has also demonstrateda maternaleffect in other species, includingNicotiana (89) andBrassica (150), but it shows no maternaleffect in Safflower (94) or in Melandriumalbum (99). In maize, maternal cytoplasmic effects have been found for adult plant height and ear height (61). For some yield charactersin this species, an interactionof cytoplasmic effects with the genotype and environmentof the offspring have also been demonstrated(56). The percentageof oil and protein content of maize kernels showed a reciprocaleffect which was not consistent over two generations(61). Garwoodet al (61) suggestedthatthis was due to a physiological influence (phenotypicmaternaleffect) ratherthana cytoplasmic effect. PATERNAL EFFECTS Passing referencehas been made a numberof times to paternaleffects (i.e. an additionalcontributionof the paternal parentto the phenotypeof the offspring beyond the nuclearzygotic contribution).These effects have been found, for example, for seed size in corn (102), soybean (90), wheat (13), and pearl millet (15, 16). In a series of crosses with maize, Fleming (55) demonstrated that male cytoplasm can influence the hereditaryexpression of yield characters in progeny, but these effects may be influenced by the maternalcytoplasm and by yearly interactions between cytoplasmic and environmental effects. A few plant groups, such as Oenothera and Geranium, show persistent paternalcytoplasmic inheritance(reviewedby 164). Paternaleffects in Geranium have recently been confirmed in a study in a naturalpopulation (135). The existence of these effects is importantfor the interpretationof cytoplasmic studies, and it cautions against the assumptionthat any and all reciprocaldifferences are due to maternaleffects. It is important,therefore,to test the relative importanceof maternalor paternalinfluences (165). DISCUSSION The generalpatternwhich has emergedto date is thatat the seed stage, a large proportionof the variationis undermaternalcontrol, and this maternalcontrol appearsto have a large environmentalcomponent.These effects carrythrough to the early seedling stages, but at the late seedling stage, the genotype of the offspring itself begins to contributesignificantly to the variation.Endosperm maternal effects and most phenotypic maternal effects have their major influence via the seed or seed structure.Cytoplasmic inheritanceis the only mechanism for direct maternaleffects on adult traits, althoughthere may be indirectcarryovereffects from the seed or seedling stage. It is not surprising 226 ROACH& WULFF therefore that the influence of maternaleffects diminishes later in the life cycle. Because maternaleffects at the adult stage may be important, they cannot be ignored in breeding programs, and they may have important consequences for fitness in naturalpopulations. This review of the evidence has revealed two large gaps in the types of studies done on maternaleffects. First, a detailed separationof the causes of maternaleffects still needs to be done. As outlined in Figure 1, there are, beyond the maternalzygotic contribution,several ways in which the maternal parent can influence the juvenile phenotype. With few exceptions, these effects have not been separated,and thus, the exact cause of the differential contributionfrom the maternalparent is not known. The second discontinuityin our review is the lack of studies on noncultivated species in natural populations. Studies in natural populations have demonstratedthatenvironmentalvariablescan have an importantinfluenceon seed size and germination,therehave been few genetic studies, however, and no conclusive identification has been made of the specific causes of the maternaleffects. In 1963, Cockerham(26) suggested that maternaleffects in plants were minimal and did not generally require consideration. From the evidence presentedhere it is clear that maternaleffects can have a significanteffect on the phenotypeof an individual.Therefore,for many types of evolutionaryand ecological studies it will be importantto consider this type of variation. Failure to consider the contributionof maternaleffects to the phenotype of individualscan lead to erroneousinterpretationsof experimentalresults. This was clearly demonstratedin a series of studies with Loliumperenne. In the first study, withoutreciprocals,Hayward& Breese (75) found that for certain traits there were high levels of dominance and interaction.However, a later study using a full diallel analysis showed reciprocaldifferencesfor these same traits and demonstratedthat the earlier results were a reflection of a high maternalcomponent (58). Quantitativestudies designed to identify maternal effects clearly can increase our ability to understandprocesses within plant populations. Unfortunately, it may be difficult to predict the importanceof maternal effects for a particularspecies. Studies have shown that for closely related species, and even within one species, there are no consistent patterns of maternaleffects for the same trait(44, 45). Two studies with Loliumperenne showed the mean values of seed weight to be exclusively under maternal control (10, 157); but in a later study with the same species, seed weight showed no maternaleffect, only additive genetic control (160). There is no reasonto expect thatthe same controls should operatein differentpopulations of a species, or in similar populations in dissimilar environments (161). Different species, and different individuals within a population, may react differently to the same maternalenvironmentaltreatments,for example, via MATERNAL EFFECTSIN PLANTS 227 interactions between maternal effects and progeny genotype (3, 4, 105). Thus, generalizationsaboutmaternaleffects acrosspopulationsor even across genotypes are not easy. One of the difficult questionsin ecological or quantitativegenetic studies in naturalpopulationsis how to study maternaleffects. Very often one does not have the time or facilities to do the crosses requiredfor complete genetic analysis of these effects. As an alternative, seed weight is often used as an estimate of maternaleffects in ecological (143) and agriculturalstudies (1, )66). A number of experimental studies (cited earlier in this paper) have demonstratedthat changing the environmentof the mother has a significant effect on the size of the seed produced. It is assumed that if there is a correlationbetween seed weight and traits expressed later in the life cycle, then there is evidence for maternaleffects (143). Sometimesmean seed size is highly correlated with maternal ability (97, 112). However, this may not always be the case. In studies using seed weight as an estimate of maternal effects, it must be recognized that maternalinfluences will be underestimated because this technique ignores other causes of maternal effects, including nutritionaldifferences and cytoplasmic inheritance(Figure 1). Some studies have shown significant maternaleffects on traits despite the absence of any correlationwith seed size (29, 43, 159). Moreover, the effect of seed size is often confined to the early growth stages (103, 158); therefore, seed weight cannot be used to estimate maternaleffects for late-life traits. Environmental studies, done under controlled experimental conditions, have clearly demonstratedthatphenotypicmaternaleffects can be caused by a numberof differentenvironmentalfactors. Seed size, for example, has shown a sensitivity to maternaltemperature,wateravailability,resourceavailability, and hormone level. These environmentalconditions will fluctuate during a growing season, and the importanceof these factors may be reflected in the variationin seed weight observed within a growing season (20, 58, 59, 136). The importanceof this variation may be similarly reflected in within-plant positional effects on seed size, when seeds in differentpositions are exposed to differentlevels of resources(1 10). Whereasstudies in a controlledenvironment can identify one particularmaternalenvironmentalfactor which may have an influence on the juvenile phenotype, it is hard to make the link between controlledand field experimentsbecause it is difficult to identify the small-scale heterogeneityperceived by an individualplant in the field. It has been shown that small-scale heterogeneitycan be importantin field studies (70, 71, 135). Not only is this scale of environmentalheterogeneityhard to measure, but the relevant scale of heterogeneity may change for different stages of the life cycle (135). Experiments need to be done to identify precisely the environmental causes and consequences of maternal effects under natural conditions. It is clear from this review that maternaleffects can confuse the interpreta- 228 ROACH& WULFF tion of genetic studies (1 16). When maternalhalf-sibshipsare used in quantitative genetic studies, maternal effects will yield biased estimates of heritability(51) and may lead one to conclude falsely that there is heritable variation in a population. A false prediction concerning the response to selection may also occur for the opposite reason. In an experimentalstudy with mice, Falconer (52) found a strong response to selection for litter size despite zero heritabilityfor this trait.Furtherexaminationof this traitrevealed a strongmaternaleffect, which explainedhis observedresults. Simple maternal effects will always inflate variation between families while having no effect on variances within families. However, the variance within families will be inflated if there is an interaction between progeny genotype and maternaleffect (106). The type of maternaleffect (Figure 1), the covariance between maternaland offspringeffects (38, 170, 178), and the persistenceof these effects throughsuccessive generations(3, 134, 179) will all influence the interpretationof selection studies. In addition to the need for more experimentalwork to identify these effects, more theoreticalanalysis of the evolutionarysignificance of maternaleffects and maternalinteractioneffects is needed. As a consequence of maternaleffects, not only does the maternalparent have a greaterinfluence than the paternalparenton the offspring phenotype, but the maternalphenotypemay for some traitsalso have a greaterinfluence than the offspring on the offspring's own phenotype. For example, seed germinationappearsto be almost exclusively undermaternalcontrol, via the seed coat or other structures(referencescited earlier). A conflict between the parent and offspring may develop: while for an individual offspring it is always advantageousto germinateearly, the parentalgenotype may favor a delay in germinationin orderto reduceoffspringcompetition(50) or to ensure success of offspring in a temporallyheterogeneousenvironment(177). The evolution of the integuments and endosperm has also been discussed as a mechanism that allows mothers increased control over the distributionof maternalinvestment to embryos, because the mother can respond to differences in vigor of early growth among offspring genotypes (178). It is clear, that maternal effects mny have had important cansequences during the evofu- tion of many traitsand may be criticalto our understandingof ecological and genetic mechanisms in present-daypopulations. ACKNOWLEDGMENTS We would like to thank H. M. Alexander, J. Antonovics, M. Hayward, A. Lubbers,M. Price, and J. Schmitt, for theirconstructivecommentson earlier drafts of this paper. 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