Evolutionary Patterns and Biogeochemical Significance of Angiosperm Root Traits

13 Pages·2012·0.5 MB·English

Evolutionary Patterns and Biogeochemical Significance of Angiosperm Root Traits
Author(s): L. H. Comas, K. E. Mueller, L. L. Taylor, P. E. Midford, H. S. Callahan, and D. J.
Beerling
Reviewed work(s):
Source: International Journal of Plant Sciences, Vol. 173, No. 6 (July/August 2012), pp. 584-
595
Published by: The University of Chicago Press
Stable URL: http://www.jstor.org/stable/10.1086/665823 .
Accessed: 31/07/2012 23:58
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp
.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact [email protected].
.
The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to
International Journal of Plant Sciences.
http://www.jstor.org
Int.J.PlantSci.173(6):584–595.2012.
(cid:2)2012byTheUniversityofChicago.Allrightsreserved.
1058-5893/2012/17306-0004$15.00 DOI:10.1086/665823
EVOLUTIONARY PATTERNS AND BIOGEOCHEMICAL SIGNIFICANCE
OF ANGIOSPERM ROOT TRAITS
L.H. Comas,1,2,* K.E. Mueller,1,yL.L.Taylor,1,zP.E.Midford,§ H. S.Callahan,k andD.J. Beerlingz
*USDA-ARS,WaterManagementResearch,FortCollins,Colorado80526,U.S.A.;yDepartmentofEcology,Evolution,andBehavior,
UniversityofMinnesota,St.Paul,Minnesota55108,U.S.A.;zDepartmentofAnimalandPlantSciences,UniversityofSheffield,
SheffieldS102TN,UnitedKingdom;§NationalEvolutionarySynthesisCenter,DukeUniversity,Durham,
NorthCarolina27705,U.S.A.;andkDepartmentofBiologicalSciences,BarnardCollege,
ColumbiaUniversity,NewYork,NewYork10027,U.S.A.
Onthebasisofasynthesisofrecentprogressinbelowgroundecology,weadvanceanddiscussahypothesis
that relates root trait evolution to the increased dominance of angiosperms into dry upland habitats and the
decline of atmospheric CO concentration that began in the Cretaceous. Our hypothesis is built from
2
examiningpatternsoffinerootadaptationsduringtheCretaceous,whenangiospermsdramaticallydiversified
in association with arbuscular and ectomycorrhizal root-fungal symbionts. We then explore the potential
effects of root adaptations and mycorrhizas on the geochemical carbon cycle. On the basis of phylogenetic
analysesofroottraitsamongextantplantspecies,wesuggestthatangiospermtaxa,whichdiversifiedsincethe
earlyCretaceous,evolvedthinnerrootswithgreaterrootlengthperunitofbiomassinvested(i.e.,specificroot
length[SRL])thanearlierdivergingtaxa.Wesuggestthatthesechangesinrootmorphologywerefacilitatedby
adeclineinatmosphericCO ,whichlikelycausedwatertobecomemorelimitingandnutrientsmoreboundto
2
organicmatter.Undertheseconditions,wesuggestthatthinrootswithlongSRLwouldhaveallowedplantsto
more efficiently forage for soil water and nutrients. This assertion is supported by the observation that SRL
correlates with greater root length density in soil and increased root capacity to take up water. Simulations
indicate that the evolution of angiosperm root systems with greater SRL and ectomycorrhizas during the
Cretaceous and Cenozoic substantially increased mineral weathering rates, with a fourfold increase in SRL,
equivalent to a quadrupling of atmospheric CO concentration. The hypothesis presented here raises the
2
possibilitythatplanthydraulicstatusandnutrientbalancetogethershapedwhole-plantgrowthstrategies,with
importantconsequences for theevolution ofthe biosphere.
Keywords: specific root length, root trait evolution, biogeochemical weathering, EM colonization, AM
colonization, nitrogen,carbondioxide (CO ),soil.
2
Introduction (1) major evolutionary patterns of plant traits, (2) the role
andidentityofkeyenvironmentalfactorsthathaveshaped
Terrestrialplants,theatmosphere,andthebiospherecoevolved these traits, (3) how shifts in root traits correlated with
over geologic time (Beerling and Berner 2005). Plant func- trait shifts in leaves and flowers and with plant nutrient and
tional traits played an important role in this coevolution by water requirements, and (4) how different traits and taxa
controlling plant responses to environmental variation and influence ecosystem functioning. Although progress has been
governingbiologicalimpactsonecosystemprocesses, suchas made in understanding the functional significance and evolu-
the sequestration of carbon, cycling of soil nutrients, weath- tionary patterns of aboveground plant traits (Reich et al.
ering of minerals, and soil formation (Verboom and Pate 2003;Wrightetal.2004;Boyceetal.2009;Feildetal.2009;
2006). To improve our understanding of plant-biosphere in- Little et al. 2010), much less is known about the ecological
teractions in the past and to better predict the outcome of andevolutionarysignificanceofbelowgroundtraitvariation.
theseinteractionsinthefuture,weneedto betterunderstand This review focuses specifically on evolutionary patterns of
fine root traits of woody forest species and how shifts in the
roottraitsofconifersandangiospermsmayhaveaffectedbio-
1Theseauthorscontributedequallytothiswork.Correspondence geochemical processes during the Cretaceous (;145–65 mil-
relatedtoroottraitsandphylogeneticsignalscanbedirectedtoL.H. lion years ago), a critical time of woody plant and biosphere
Comas([email protected]),rootfunctioninginpaleoclimates evolution. We emphasizewoodyforestspecies for several rea-
to K. E. Mueller ([email protected]), and biogeochemical sons. First,several woodyplantlineages diversified duringthe
weatheringtoL.L.Taylor(l.l.taylor@sheffield.ac.uk). Cretaceous. Second, forests composed of these lineages have
2Authorforcorrespondence;e-mail:[email protected].
played a dominant role in driving terrestrial biogeochemical
Manuscript received October 2011; revised manuscript received February cycles over this time compared with grasslands and savannas,
2012. which are more recent (Beerling and Osborne 2006; Tipple
584
COMAS ETAL.—ANGIOSPERM ROOT TRAITS 585
and Pagani 2007; Stro¨mberg 2011). Third, a broad analysis protocols for appropriate field sampling have allowed for the
that includes herbaceous plants is currently hindered in part collectionofimproveddatasetsforcomparativeanalyses.
by methodological issues. Specifically, measurements of trait Currently, there are limited data on a broad range of root
variation among woody plants have recently focused on the traits and species to facilitate extensive evaluation. Conse-
most distal root branches (i.e., ephemeral roots specialized quently,keyroottraitsassociatedwithplantgrowthstrategies
forsoilresourceacquisitiondistinctfrom woodyroots),while are poorly resolved. Studies of root functional ecology have
herbaceous root traits are typically measured on the entire emphasized morphological and physiological variables, such
rootsystem,perhapsbecausethereismoreoverlapamongsec- asspecificrootlength(SRL;rootlengthperunitbiomass)and
tions of the root system in functions such as soil resource nitrogen (N) concentration, that reflect resource deployment
acquisition, transport, anchorage, and storage (perennial her- infineroottissues(Eissenstatetal.2000).Inprinciple,SRLis
baceous plants). Other researchers are conducting work with governed by a combination of morphological traits, particu-
roots of herbaceous annuals and perennials (Grime et al. larly root diameter and tissue density, that affect the amount
1997; Craine et al. 2002; Levang-Brilz and Biondini 2003; of root length deployed per unit root biomass (Fitter 1991).
Tjoelker et al. 2005; Roumet et al. 2006; Kembel and Cahill However,thusfar,differencesinSRLamongwoodyplantspe-
2011), and it may eventually be possible to synthesize data cies are generally found to be associated with species differ-
morebroadly. ences in root diameter rather than tissue density (Comas and
Here,wefirstprovideanoverviewoffinerootmorpholog- Eissenstat2004,2009).Certaintraits,suchasroottissueden-
ical and functional traits of woody plants and then evaluate sity and root hair density, may vary less consistently among
links between fine root morphology, function, and plant woodyspeciesandbestronglyinfluencedbysoilmoisturecon-
growth strategies. These links are critical for interpreting ditions (Comas and Eissenstat 2009; Holdaway et al. 2011;
the significance of evolutionary patterns in root traits, which L.H.ComasandH.S.Callahan,personalobservation).Other
we subsequently explore. Given the paucity of the fossil key traits, such as root life span and root length density
record for plant roots and mycorrhizas (Peterson 1992), we (RLD) per soil volume, are rarelymeasured but are central to
emphasize phylogenetically informed comparisons of extant a plant’s ability to forage for soil nutrients. This is partly be-
taxa as a promising strategy for advancing large-scale eco- causeitismoretimeconsumingtomeasurerootlifespanand
logical understanding (Westoby 2006). Finally, we describe RLD and because these traits are more difficult to measure at
a novel, broad hypothesis that relates root trait evolution thespecieslevelinmixedforests.
tothedeclineofatmospheric CO concentrationthat began Commonly measured traits of fine roots, such as SRL and
2
in the Cretaceous. We consider potential effects of root ad- rootN concentration,closelymirrorleaf traits emphasizedby
aptations on biogeochemical processes during and since the studiesoffunctionalecology(e.g.,specificleafareaandleafN
Cretaceous using a combination of theory, observations concentration; Wright et al. 2004), but roots differ in several
from modern ecosystems, and simulations of mineral weather- ways that add a layer of complexity to discussions of their
ing rates (Taylor et al. 2011, 2012). Our overarching aim functionaltraitsandpotentialtrade-offs.First,inthemajority
is to integrate studies of plant traits with ecosystem-scale ofplants,rootsformsymbioseswithoneormoretypesofmy-
processes (Allen and Hoekstra 1992) as a necessary step corrhizalfungithataredirectlyinvolvedinsoilresourceacqui-
for better understanding the coevolution of plants and the sition, especially of phosphorus (P) and N (Smith and Read
biosphere. 2008).Differenttypesofmycorrhizalfungi,suchasectomy-
corrhizal and arbuscular mycorrhizal fungi (EM and AM,
respectively), also likely exert unique selection pressures on
plants—and root traits specifically—because of differences in
Fine Root Form and Function: A Primer their ownfunction and morphology (Brundrett 2002;Comas
andEissenstat2009).Next,whileleaftraitevolutionislargely
Short-livedtissuesthatprimarilyfunctioninresourceacqui- driven to maximize carbon (C) fixation while minimizing wa-
sition, such as leaves and nonwoody fine roots, represent ter loss (Boyce et al. 2009; Feild et al. 2011a), roots provide
a considerable plant investment of mineral nutrients and bio- awidearrayoffunctions,suchasdirectrootuptakeofsoilre-
massfortheirconstructionandmaintenance.Recentworkhas sources and support of mycorrhizal fungi, that cannot neces-
progressedincharacterizingfinerootsystemsofwoodyplants sarily be simultaneously maximized (Brundrett 2002). Finally,
with greater clarity and precision. Fine roots specifically refer different strategies are likely required to maximize acquisition
to thin and highly branched, distal root clusters that function of limiting soil resources that differ in spatial distribution and
to forage for and absorb soil resources (Pregitzer 2002; Xia mobility. For example, it has been suggested that immobile
et al. 2010). These nonwoody roots, typically the youngest nutrientsaremosteffectivelyforagedbyplantssupportingmy-
and thinnest branches (first and second order, counting back corrhizal colonizationorroothairs andhighly branchedroots
from root tips; Pregitzer 2002), are distinct from more con- for extensive foraging (Brundrett 2002). In contrast, mobile
spicuous roots that undergo secondary cambial growth and nutrients and water may be more effectively foraged with in-
function for storage and anchorage (Esau 1977; Comas et al. creasedrootsurfaceareaandlocalizedproliferation(Robinson
2002; Pregitzer 2002; Guo et al. 2008). The ephemeral por- etal.1999;Brundrett2002).Nonetheless,predictablepatterns
tion of the root systems is comprised of the finest two root in root trait variation, reflecting adaptations to selective pres-
branch orders (Xia et al. 2010). Although it is challenging sures over geologictime, areexpected onthe basis of theories
to collect data on this portion of the root system, improved ofplant strategiesrelatedtoplantresource acquisitionandal-
definitions of the fine root system and the standardization of locationandareworthexploring.
586 INTERNATIONAL JOURNAL OF PLANTSCIENCES
Optimization of Root Form and Function: cases, low root tissue density (Comas et al. 2002; Paz 2003;
Perspectives on Root Trait Adaptation Zangaroet al. 2007; Holdaway etal. 2011).Across commu-
nities varying in nutrient availability, species adapted to low-
Root Traits and Plant Growth Strategies nutrient conditions also had thinner roots with longer SRL
andgreaterorinsignificantlydifferentroottissuedensity,po-
Root morphological traits can vary widely (by a difference
tentially enhancing foraging of limited nutrients (Paz 2003;
ofanorderofmagnitude)amongplantspeciesacrosscommu-
Holdawayetal.2011).
nities (temperate rainforest chronosequence: Holdaway et al.
LongerSRLamongcontrastingspecieshasbeenassociated
2011)aswellaswithincommunities(temperateforest:Brundrett
with greater metabolic activity and higher rates of nutrient
and Kendrick 1990; Pregitzer et al. 2002; Withington et al.
uptake (Comas et al. 2002; Holdaway et al. 2011; but see
2006; Guo et al. 2008; Comas and Eissenstat 2009; tropical
Comas and Eissenstat 2004) but also higher respiration rates
forest:St.John1980;Paz2003;Zangaroetal.2007).Varia-
andtissueNconcentrations(Comasetal.2002;Volderetal.
tion in root morphology is linked to whole-plant growth
2005). Long SRL among contrasting species has been associ-
strategies (Reich et al. 1998; Comas etal. 2002) that are op-
ated with fast-growing roots (Eissenstat 1991) and shoots
timized for success in different environments (Tilman 1988;
(Comasetal.2002;Nicotraetal.2002;ComasandEissenstat
Lambers and Poorter 1992; Chapin et al. 1993; Westoby
2004), but there are exceptions. Some fast-growing species
1998; Grime 2001). It has been noted that root diameter is
have short SRL, perhaps due to optimization of root tissue
oftenthinnerandSRLgreaterinangiospermsthaningymno-
to maximize nutrient uptake through symbiotic interactions
sperms (Reich et al. 1998; Bauhus and Messier 1999; Osto-
with fungi instead of directly through root uptake (Comas
nen et al. 2007; Alvarez-Uria and Ko¨rner 2011). However,
et al. 2002; Comas and Eissenstat 2004). Finally, root mor-
species of early diverging angiosperm lineages, such as Mag-
phology and physiology have been predicted to vary in con-
noliids, have coarser roots with lower SRL than gymno-
cert with root longevity in relation to whole-plant growth
sperms (Pregitzer et al. 2002; Comas and Eissenstat 2009).
strategy,suchthatinvestmentinrootsisoptimizedrelativeto
Further, much like specific leaf area, SRL and root diameter
resource uptake (Eissenstat and Yanai 1997). However, SRL
may constrain variation in other functional traits—in particu-
can be uncoupled to root life span (Withington et al. 2006;
lar,rootphysiologyandlifespan—butthenatureoftrade-offs
Espeleta et al. 2009), for example, when traits such as thick-
betweenmorphologyandrootfunctionsispoorlyunderstood.
ness of outer tangential exodermis walls are more closely as-
Emerging evidence associates root morphology with plant
sociated with root life span than SRL (Withington et al.
strategies for acquiring limited supplies of water. For exam-
2006).
ple,thinnerrootswithareducedcorticalarealikelyhaveless
Finally, root morphology can impact the nature of sym-
impedance to water movement (Eissenstat and Achor 1999),
bioses between plants and mycorrhizal fungi. Thin root
and species with thinner roots and longer SRL appear to
diameters and long SRL potentially limit colonization by
have greater hydraulic conductivity both within a genus
mycorrhizalfungi,particularlyAMfungi,becausetheyhave
(Huang and Eissenstat 2000; Solari et al. 2006) as well as a reduced cortical area per length to support mycorrhizal
across broad species comparisons (Rieger and Litvin 1999; associations (Baylis 1975; St. John 1980; Graham and Eis-
Herna´ndez et al. 2009). Among several temperate woody senstat1998;Brundrett2002).Suchrelationshipshavebeen
genera—including Quercus, Carya, Betula, Populus, and used to suggest that plants with thick roots and short SRL,
Aralia—specieswiththinnerrootsandgreaterSRLweregen- which are also associated with slow elongation rates (Eis-
erallyassociatedwithmorexerichabitats,potentiallytoabet senstat 1991), are dependent on fungal symbionts for nutri-
wateruptake(EspeletaandDonovan2002;L.H.Comasand ent foraging (Baylis 1972, 1975). However, thin roots with
H. S. Callahan, unpublished data). SRL of species increased longSRLmayhavegreatersurfaceareapermasstointeract
as soil moisture decreased across several sites in the Amazon with symbiotic fungi and more root length to intersect
rainforest (Metcalfe et al. 2008). Likewise, roots were thin- symbiotic fungi in the soil matrix, as some studies have
nerandspecific rootareagreater in Fagussylvaticastandsin found greater AM mycorrhizal colonization on thinner
Germany as precipitation declined (Meier and Leuschner roots (Siqueira and Saggin-Junior 2001; Roumet et al.
2008). Finally, SRL and hydraulic conductivity were posi- 2006; Zangaro et al. 2007). These studies potentially also
tively related to photosynthetic rates among species adapted reflect the tendency of thinner roots to grow more quickly
to xeric conditions, suggesting that root form and function- and be colonized earlier (Roumet et al. 2006), although
ing matter for growth when water is limiting (Herna´ndez mycorrhizal colonization rates are presumably regulated by
etal.2009). activesignalingmechanismsevolvedbetweenrootsandfungi
Root morphology, especially SRL, is predicted by theoreti- to control colonization (Graham et al. 1991). EM coloni-
cal solute transport models to be important for nutrient for- zation has rarely been examined in association with root
aging(EissenstatandYanai1997).Increasingrootlengthand morphology and may be independent of morphological con-
root surface area in soil is more effective for soil nutrient straints because EM associations form at root tips. Interest-
acquisition than simply increased root biomass (Eissenstat ingly, L. H. Comas (unpublished data) found less root tip
1991; Fitter 1991). Trait patterns revealed in comparative colonization by EM fungi on hosts with thinner root diame-
studies generally support this view. For example, fast-growing ter and longer SRL, supporting the hypothesis that hosts
or early successional species, which theoretically need faster withthinnerroots andlongerSRLmayhaveevolvedlessde-
nutrient uptake, were associated with root morphological pendency on mycorrhizas. That is, if the benefits that plants
traitssuchaslongerSRL,thinnerrootdiameters,and,insome derive from fungal partners do not compensate for the cost
COMAS ETAL.—ANGIOSPERM ROOT TRAITS 587
ofsupportingthem, theremaybe naturalselectionforplants
toactivelydownregulatetheextentofrootcolonization.
For several reasons, universal correlations may be un-
likelybetweentraitsthatenhanceresourceuptakeefficiency,
such as thin root diameter, longer SRL, low N concentra-
tion,andlongrootlifespan.First,thenumberofroottraits
related to efficient resource allocation suggests that optimal
plantinvestmentinabsorptiverootscanbeachievedbysev-
eral different combinations of trait values. Second, the effi-
ciency of any given trait value or combination of traits also
depends on the scope of investment in roots, as reflected
by RLD and the extent of soil volume exploited by roots
(Eissenstat et al. 2000). In other words, efficiency may be
determined not just by the morphological and functional
traits of individual fine roots but also by the quantity and
spatial extent of root length in soil. Finally, simple predic-
tionsoftrade-offsamongroottraitsandtissueoptimization
for resource acquisition are complicated by interactions be-
tweenfinerootsandmycorrhizas.
In summary, a plant’s competitive ability for acquiring soil
resources is largely determined by the total length and sur-
faceareaofitsrootsandmycorrhizasaswellasthetotalvol-
Fig. 1 Relationshipbetween specific root length (SRL) and root
ume of soil it can explore. Plant uptake of resources is likely
lengthdensity(RLD)insoiloffirst-andsecond-orderterminalroots
jointly constrained by root morphology, metabolic activity,
from11temperateforesttreesgrowninacommongardenincentral
and root tissue longevity, such that the efficiency gained by
Poland (Withington et al. 2006). Species represented include five
one trait (e.g., thin diameter, long SRL, or long life span)
hardwoods(graycircles;AcerpseudoplatanusL.,AcerplatanoidesL.,
could allow for greater investment in root length or mycor- FagussylvaticaL.,QuercusroburL.,andTiliacordataMill.)andsix
rhizalassociations.Explorationintothesetrade-offshasbeen conifers (black circles; Abies alba Mill., Larix decidua Mill., Picea
limited but is crucial for understanding trait patterns. Data abies (L.) Karst., Pinus nigra Arnold, Pinus sylvestris L., and
from a commongarden experiment of temperate trees shows Pseudotsuga menziesii (Mirbel) Franco). The dotted line indicates
that species with longer SRL (i.e., less biomass investment RLD as a function of ln-transformed SRL, excluding one point
per unit root length) tend to have greater RLD (fig. 1). Con- (F.sylvatica;thickgraycircle;R2¼0:69,P<0:05).Alogarithmicfit
that includes F. sylvatica was also significant (R2¼0:41, P<0:05).
versely,greater dependence onmycorrhizal fungifor nutrient
Consistent with this relationship and the relationship between root
acquisitioncouldnecessitatelimitsonbiomassinvestmentsin
diameterandSRL,rootdiameterwasalsonegativelycorrelatedwith
fine roots, for example, through lower RLD. The form of
RLD(R2¼0:37,P<0:05;datanotshown).
thesetrade-offsthatismostbeneficialtoplants(i.e.,theopti-
mal combination of root traits) likely depends on the nature
of available soil resources, which is a function of climate, Baylis (1972, 1975) first suggested that recent plant radia-
soilproperties,andbiota. tions resulted in species evolving thinner roots and long root
hairs. He hypothesized that this evolutionary pattern was
driven by benefits of less dependency on mycorrhizas, which
require substantial C support of fungi by plants (Peng et al.
Phylogenetic Patterns of Root Trait Variation
1993; Graham and Eissenstat 1998). This hypothesis was
Becauseofthescarcityoffossilrootsandmycorrhizasdur- founded on weak projections of root trait patterns (extrapo-
ing the Cretaceous, the geologic record has not produced lated from Magnoliid vs. grass root traits) and a simplistic
a detailed picture of root trait evolution during the most im- view of plant-fungal interactions but has inspired investiga-
portant period of angiosperm diversification. A powerful ap- tions into root trait patterns. Baylis partially supported his
proach to filling this knowledge gap is to examine trait hypotheses with observations that extant species that are
variationamonglivingplantsinthecontextoftheirphyloge- nonmycorrhizal or facultatively mycorrhizal have thin roots
netic history (Peterson 1992). The emerging pattern from with dense numbers of thin root hairs (Baylis 1972, 1975).
phylogenetic analyses of extant angiosperms and gymno- These observations have been supported by others, although
sperms suggests that basal angiosperms had relatively coarse nonmycorrhizal or facultatively mycorrhizal plants are often
roots and shortSRL butthatangiosperm lineagesdiversifying special cases, limited either to a few rare cases of plants
more recently during the Cretaceous had finer roots (Comas adapted to extreme habitats—such as Cyperaceae and
andEissenstat2009;L.H.ComasandH.S.Callahan,unpub- Proteacea—or to short-lived herbaceous vegetation, such as
lished data; figs. 2, 3). However, this evolutionary interpreta- Brassicaceae (Peat and Fitter 1993; Lambers et al. 2008;
tion necessitates the assumption that trait differences among Brundrett2009).
extant species mirror the patterns of their ancestors, which Pregitzer et al. (2002) reported large interspecific variation
should be tested with fossil evidence when available (Feild in root morphology among nine North American species
etal.2011b). and, consistent with the suggestions of Baylis, noted an evo-
588 INTERNATIONAL JOURNAL OF PLANTSCIENCES
Fig.2 Diameter(mm)ofrootsfunctioninginsoilresourceacquisition(i.e.,clustersoffirst-andsecond-orderroottips)reconstructedalong
phylogeneticlinesamong20tropicalandsubtropicalangiospermsandsomeoftheirnearestextantnonseedplantlineages.Thephylogenictreeis
basedonrecentanalysesofplanttaxa,withbranchlengthsindicatingproximityofrelationshipsinunitsofmillionsofyears,asestimatedwith
maximumlikelihoodmethods(Wikstrometal.2001;MagallonandSanderson2005).Speciesinclude16angiosperms(Austrobaileya–Ficus)and
fournonangiospermseedplants.Branchcolorindicatesrootdiameterofeachspeciesandnode,withvaluesatnodesestimatedwithsquared-
changeparsimony(Mesquite2.75;MaddisonandMaddison2010).
lutionary pattern across conifer, magnoliid, and eudicot ary pattern was found of first- and second-order roots be-
clades for roots to have evolved greater SRL and decreased coming thinner as seed plants diverged from basal lineages
diameter.Examiningrootmorphologyacrossabroadertaxo- (e.g., cycads, gnetophytes, Gingko) through recent angio-
nomicrangeofspecies(25temperatewoodytaxa)withinthe sperm clades (figs. 2, 3). Among angiosperms alone, this
same forest community, Comas and Eissenstat (2009) found data set showed a 20-fold difference in SRL, spanning the
a 10-fold difference in SRL among angiosperms spanning sameintervalofdiversification.Inseveralcases,rootdiame-
;140millionyearsofspeciesdiversification.Acrossabroader ter of basal angiosperms overlapped with basal seed plant
phylogeny in a data set of 20 tropical and subtropical species lineages (Comas and Eissenstat 2009; L. H. Comas and
sampled from plants in botanical collections, an evolution- H.S.Callahan,unpublisheddata;figs.2,3).Withintemper-
COMAS ETAL.—ANGIOSPERM ROOT TRAITS 589
ring during the Cretaceous? We hypothesize that one impor-
tant effect on root trait evolution was the long-term drop in
atmosphericCO concentrationthatbeganduringtheCreta-
2
ceous and continued until ;20 million years ago (Royer
2006; Fletcher et al. 2008). This decline in CO concentra-
2
tion would have increased substrate limitation of photosyn-
thesis.Inangiosperms,thisconstraintonphotosynthesismay
have been partly alleviated by the evolution of progressively
higher leaf stomatal and vein densities to allow greater rates
ofleafCO uptake(BeerlingandFranks2010;Brodribband
2
Feild 2010; Feild et al. 2011a). To support the greater water
losses required to achieve high leaf vein density and photo-
synthetic rates as CO concentration potentially declined,
2
selection would likely favor evolution of root traits that
maximized water uptake and transport by roots while mini-
mizing energetic investmentin root construction andmainte-
nance. In this context, thin roots with greater SRL could
havebeenadvantageouscomparedwiththick,denserootsby
Fig. 3 Reconstructedroot diameter as a function of time in mil- enabling plants to efficiently increase the volume of soil that
lionsofyearsfromeachnodetotherootofthephylogenetictreefor could be explored (i.e., RLD; fig. 1) and the hydraulic con-
the20tropicalandsubtropicalspeciesinfig.2.Pointsrepresentthe ductance of root systems (Eissenstat and Achor 1999; Rieger
19nodes amongthe20 species.Therootof thetree is 0. Thesolid and Litvin 1999; Huang and Eissenstat 2000; Solari et al.
line indicatesa significantdecrease in rootdiameterwith timefrom
2006;Herna´ndezetal.2009).
therootofthetree(R2¼0:83,P<0:001).
Advancements in water acquisition and transport may
haveallowedearlyangiospermstoescapethewethabitatsof
their ancestors and diversify into more xeric and open habi-
ate forest communities, recently diverged lineages were
tats previously dominated by ferns and lycophytes (Feild and
not uniformly fine rooted but included some species with
Arens 2007). Changes in belowground traits may have oc-
coarser roots (Comas and Eissenstat 2009; L. H. Comas
curred in conjunction with aboveground traits, such as in-
and H. S. Callahan, unpublished data). Interestingly, these
creases in leaf photosynthetic capacity (Boyce et al. 2009;
species often had other strategies for competing for re-
Feild et al. 2009; Brodribb and Feild 2010). Species with
sources, such as allelopathy in Juglans nigra (Comas and
thinner roots and longer SRL may be more competitive in
Eissenstat 2009). Recently diverged angiosperm lineages also
novel habitats (i.e., be more weedy), especially if coevolved
include species with some of the finest roots that exist, such
mycorrhizal fungi are absent or limited. Weedy herbaceous
as ericaceous plants that have roots finer than human hair
specieshavebeenassociatedwithlongerSRLthannonweedy
(Valenzuela-Estradaetal.2008).
species (Wright et al. 1999). Nonmycorrhizal or facultatively
mycorrhizal species can be associated with highly disturbed
Interactions among Woody Root Traits, Environmental habitats that can limit the development of extensive mycor-
Change, and Biogeochemical Processes since the rhizal networks (Malloch et al. 1980; Fitter and Moyersoen
Early Cretaceous 1996;Brundrett2002).
Declining CO concentration from the Cretaceous onward
2
Several woody plant taxa—including some of the best- could have favored evolution of thin roots with long SRL as
studied taxa with respect to root traits, such as temperate a result of its indirect effects on soil nutrient availability. As
tree species—diversified during the late Cretaceous and sub- climatecooled withthelong-term declineinCO concentra-
2
sequently rose to dominance (Wing and Boucher 1998). We tion (Royer 2006; Fletcher et al. 2008), reductions in soil
present a hypothesis for how environmental change shaped organic matter decomposition rates may have increasingly
root trait evolution during the Cretaceous and the potential slowed release of N and P, decreasing the availability to
implications of these trait shifts. We base the hypothesis on plants (Kirschbaum 1995; Na¨sholm et al. 1998; Smith and
the theoretical framework outlinedabove as wellas observa- Read 2008, p. 536). Such a pattern is evident across modern
tions of how current plants and ecosystems respond to envi- forests: nitrate, the most mobile form of soil N, is typically
ronmental change. We then use a model to evaluate the most abundant in the tropics, but ammonium and organic N
potential effects of root diameter and SRL on chemical min- become increasingly abundant and nitrate becomes scarce as
eral weathering and the effect of different atmospheric CO one moves poleward (Read and Perez-Moreno 2003). When
2
concentrations immobile and organic N sources are relatively abundant,
plants with traits that facilitated EM fungal associations and
efficient soil exploration—that is, thin, highly branched
Natural Selection of Woody Root Traits in the
roots—wouldlikelyhaveasuperiorcapacityforNacquisition
Context of Paleoenvironmental Change
and growth. Variation in root morphology across modern
Howmighttheevolutionofthinnerroots,higherSRL,and environmental gradients suggests that long SRL is beneficial
EMassociationshavebeenrelatedtoclimaticchangesoccur- where nutrients limit plant growth, such as at high latitudes
590 INTERNATIONAL JOURNAL OF PLANTSCIENCES
and sites with nutrient-poor soils (Ostonen et al. 2007; It has long been assumed that the spread of angiosperms
Alvarez-Uria and Ko¨rner 2011; Holdaway et al. 2011), but contributed to a decline in atmospheric CO concentration
2
morestudiesareneededtoverifythesepatterns. duringthelateCretaceous(Volk1989;BernerandKothavala
Novel EM associations in the Mesozoic likely also ben- 2001).Taylor et al.(2009) suggested that thespread of ecto-
efitedplantnutrientacquisitioninecosystemswheresubstan- mycorrhizal interactions in both angiosperm and gym-
tial proportions of nutrients were bound to organic matter. nosperm trees provided a plausible alternative—or even
It is well established that the original state of mycorrhizal complementary—mechanism for enhancing weathering over
statusinvascularplantswasAM(Brundrett2009).Although the same period. This hypothesis was later supported by
mycorrhizal formations of basal angiosperms are a big un- process-based modeling of the effects of plants and mycor-
known, the majority of extant vascular plants form AM, rhiza on terrestrial weathering regimes through the Creta-
with EM associations evolving independently in at least 12 ceous(Tayloretal.2011,2012).Here,weemploythesame
lineages that include species dominant in many important root-mycorrhizal fungal model in a sensitivity analysis to
ecosystems today (Brundrett 2009). It has been suggested explore the effects of evolutionary changes in root traits on
that EM associations evolved in concert with leaf traits, pro- silicate rock weathering (basalt and granite; figs. 2, 3). Be-
moting slower leaf litter decomposition (Cornelissen et al. cause there are many uncertainties in modeling, including
2001). Regardless, because EM fungi have a greater ability the paucity of data on roots and fungi of the Cretaceous,
to take up organic compounds (at least relative to AM) and our results should be considered illustrative rather than de-
translocate N from EM hyphae to roots (Read and Perez- finitive. Nevertheless, process-based modeling provides an
Moreno 2003; Chapman et al. 2006), EM associations are indication of the relative importance of root traits for influ-
thought to be advantageous when organic-bound nutrients encing this key control point on the long-term geochemical
are relatively abundant (Malloch et al. 1980; Brundrett carboncycle.
2002). There is also evidence that EM fungi, relative to AM We model acidification of the rhizosphere as being ulti-
fungi, stimulate soil organic matter degradation (Brzostek mately controlled by the net primary production of vegeta-
and Finzi 2011) and net N mineralization (i.e., release of in- tion, with the total influence of plants being dependent on
organicNfromorganicNsources;PhillipsandFahey2006). the spatial extent of their rooting systems in soil (Taylor
Additional advantages that EM fungi can contribute to their etal.2011,2012).Rootsandhyphaearetreatedascylinders,
hosts are that they tend to develop more extensive hyphal with root diameter, total length, and CO concentration
2
networks in soil that remain active longer into the season given as input parameters. In this simple geochemical model,
(Querejeta et al. 2007). Finally, EM fungi have several traits there is no attempt to link fine root or mycorrhizal hyphal
that likely enhanced weathering rates relative to AM, which traits to plant physiology. Rather, the aim of this modeling
may have led to competitive advantages of EM over AM is to investigate theoretical weathering effects attributable to
hosts if nutrients freed during the weathering process stimu- different root traits. Holding climate, vegetation, root bio-
latedplantgrowth(Tayloretal.2009). mass, and AM colonization constant, we estimated the ef-
fects of changes in RLD and diameter on weathering of
basalt and granite under both contemporary and Cretaceous
CO concentrations (fig. 4). To test the sensitivity of the
Effects of Root and Mycorrhizal Fungal Coevolution 2
model to rootlength in soil (fig.4A, 4C),assuming strict co-
on Mineral Weathering
variance between SRL and RLD (fig. 1), we varied SRL over
Animportantlong-termsinkforatmosphericCO concen- the range observed by Comas and Eissenstat (2009) while
2
trationisthereleaseofcalciumandmagnesiumduringchem- holding fine root diameter constant at 0.58 mm, the mean
ical weathering of two common silicate rocks, granite and value for forests (Jackson et al. 1997). To assess whether
basalt.Weatheringincreasesthecontinentalfluxesofcalcium root morphology—specifically diameter—could influence
and magnesium released from silicate rocks into the oceans weathering rates independently of RLD (i.e., assuming RLD
to form marine carbonates and remove CO from the at- is insensitive to root diameter), we varied diameter over the
2
mosphere (Berner 2004). Plants enhance silicate rock weath- range observed by Comas and Eissenstat (2009; fig. 4B, 4D)
ering by the activities of fine roots and mycorrhizal hyphae, while holding RLD constant by constraining SRL at 36 m/g,
which increase the acidity of soil in the rhizosphere through derived from average forest RLD (Jackson et al. 1997) and
respiration, nutrient uptake, and exudation of organic acids biomassscaledfromNorbyetal.(2004).Ourresultsdemon-
(Jones1998;Casarinetal.2003;Tayloretal.2009).Further- stratethatchangesinrootmorphologyarelikelytoinfluence
more, fine root and fungal activities associated with forest weathering rates through their potential effect on RLD (as
soils promote the production of pedogenic clay minerals and shown in fig. 1). Variations in root diameter per se have mi-
reduce soil erosion (Pate and Verboom 2009; Verboom et al. nor effects on weathering rates (at constant RLD and bio-
2010). Because pH is one of the most important drivers of mass; fig. 4), whereas changes in RLD exert much stronger
chemical weathering, rhizosphere soil should experience effects (at constant diameter or tissue density and biomass).
higher weathering rates than soil without roots or hyphae. Weatheringratesonbasaltwerehigherthanthoseongranite
Thus, the influences of SRL and mycorrhizal fungi on the because basalt is easier to weather and is richer in calcium
nature and extent of the rhizosphere in soils are potentially andmagnesiumthangranite.
important controls on mineral weathering rates and subse- Wealsoinvestigatedpotentialeffects ofevolutionaryshifts
quent feedbacks on atmospheric CO concentration in the in EM colonization on basalt and granite weathering by
2
longterm. broad-leaved deciduous tree species (fig. 5). We found that
COMAS ETAL.—ANGIOSPERM ROOT TRAITS 591
Fig.4 Weatheringofbasalt(A,B)andgranite(C,D)asafunctionofspecificrootlength(SRL),withdiameterheldconstantat0.58mm(A,
C), and of fine root diameter, with SRL held constant at 36 m g(cid:2)1 (B, D). These simulations show model sensitivity to independent model
parametersofSRLanddiameter.ValuesfordiameterandSRLwhenconstantwereaveragesacrosstemperateandtropicaltreesfromtheliterature
(Jacksonetal.1997).Rangeinrootlengthdensity(RLD)usedinthemodelwas2.0–8.0kmm(cid:2)2landfortemperateandtropicaltrees(Jackson
etal.1997).RLDwasconvertedtoSRLassumingastandingfinerootbiomassof150gm(cid:2)2land.OpensymbolsindicateelevatedCO (1400
2
ppm);solidsymbolsindicateambientCO (364ppm).
2
modeled weathering rates on both basalt and granite soils trient uptake by roots and mycorrhizal fungi required to
weresensitivetovariationsbetweenthenonmycorrhizalstate support the higher net primary production. This resulted in
(0%) up to 100% EM colonization (fig. 5A, 5B). Similar re- a marked increase in basalt and granite weathering rates
sultsareobtainediftheproportionofEMvegetationrelative acrossthemodeledrangeofrootmorphologyandEMcoloni-
to AM vegetation is considered (fig. 5C, 5D), representing zation compared with contemporary CO concentration (figs.
2
the evolution and spread of EM hosts at the expense of AM 4, 5). It is striking that quadrupling RLD via changes in root
hosts inthe Mesozoic. Smalldifferences between the nonmy- morphology and quadrupling atmospheric CO concentration
2
corrhizal (fig. 5C) and AM (fig. 5D) weathering (below 5% have similar effects on weathering rates, indicating that root
EM) are observed on granite but not basalt. The shapes of morphology could be an important, previously unrecognized
these curves are a complex function of geochemical controls driverofweatheringandthereforedrawdownofCO .
2
onsoilsolutionpH,whicheffectivelydictatethatEMcoloni-
zation rates under ;30% are not associated with large in-
creasesinweatheringrates. Conclusions
WefurtherinvestigatedhowhighatmosphericCO concen-
2
trations that prevailed during the Cretaceous (Fletcher et al. Root trait patterns of extant woody angiosperms suggest
2008) when angiosperm trees diversified might affect biologi- thatrootadaptationsaccompaniedthediversificationandsub-
cal weathering by roots and both types of mycorrhizal fungi sequent rise of angiosperms since the early Cretaceous. If fine
(AM and EM). An elevated atmospheric CO concentration root and mycorrhizal adaptations during the Cretaceous mir-
2
(1400 ppm CO ) increased forest net primary production by roredtraitdifferencesfoundintheirextantrelatives,roottrait
2
22% (from 5.8 to 7.11 Mg C ha(cid:2)1 yr(cid:2)1) and reduced rhizo- shifts likely allowed these angiosperms to forage for soil
spherepHby0.1–0.3pHunitsasaresultoftheincreasednu- water and nutrients more effectively. The evolution of thinner
592 INTERNATIONAL JOURNAL OF PLANTSCIENCES
Fig.5 Impactofpercentcolonizationofroottipsbyectomycorrhizalfungionweatheringratesofbasalt(A,B)andgranite(C,D).InAandC,
rootsuncolonizedbyectomycorrhizal(EM)fungiareassumedtobenonmycorrhizal,whileinBandD,rootsuncolonizedbyEMareassumedto
becolonizedbyarbuscularmycorrhizal(AM)fungi.Rootdiameterwassetat0.58mm,andat0%EMcolonization,totallengthwassetat
5400mm(cid:2)3soil.ThelengthofEMhyphaeextendingbeyondtherootsurfaceinthetoplayerofsoilwas125mcm(cid:2)3soilat100%EMroottip
colonization,andinBandD,thelengthofAMwas5cmcm(cid:2)3soilwhenEMcolonizationwas0%(Klironomosetal.1997;Tayloretal.2011).
SymbolsindicateCO concentrationsasinfig.4.
2
roots with longer SRL—and presumably high root hydraulic concentration beginning in the Cretaceous, coupled with a
capacity—in extant nonbasal angiosperm clades is consistent coolingclimate,wasacriticalfactorinshapingtheevolution
withevolutionofhighleafveindensityandphotosyntheticca- ofroottraitsandselectedforfinerdiameterrootswithlonger
pacity of these plants. The combination of plant traits (high SRLtofacilitaterootforagingfornutrientsasnutrientbecame
SRL, high root and leaf hydraulic capacity) may have been increasingly retained in organic matter. These hypotheses are
critical for expansion into novel habitats that were drier or supported by general patterns of fine root diameter of plant
more open. Root trait shifts associated with this angiosperm speciesbecomingfiner,movingfrombasaltomorerecentlydi-
rise to dominance could have accelerated mineral weathering, verged lineages over a broad phylogenetic range of angio-
complementing the faster growth rate of angiosperms and the sperms and their nearest nonseed plant relatives. Support for
increased requirement of angiosperms for soil nutrients. It is these hypotheses can also be found in observations of root
also possible that the long-term decline in atmospheric CO trait variation across environmental gradients, which indicate
2