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
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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,
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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
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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
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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
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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
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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-
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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. We would also like to thankA. Winn for many helpful
discussions with us on this subject. This paperwas writtenwhile R. D. Wulff
was on leave of absence from the UniversidadCentralde Venezuela;she was
MATERNAL EFFECTSIN PLANTS
229
supportedin partby a grantfrom Consejo de DesarrolloCientifico y Humanistico of the UniversidadCentralde Venezuela, Caracas.Special thanksto A.
Herrerawhose generouscooperation,in part, made this leave possible. D. A.
Roach was supported by NIH National Research Service Award F32AG05376 from NIA during this time.
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