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Development!Of!Tools! The$Pennsylvania$State$University$ $ The$Graduate$School$ $ College$of$Agriculture$ ! ! ! DEVELOPMENT!OF!TOOLS!TO!EVALUATE!THE!UTILITY!OF!GRAIN!LEGUME!! ! ROOT!ARCHITECTURE!! ! ! ! A$Dissertation$in$$ $ Horticulture$ $ by$$ $ James$D$Burridge$ $ $ $ ©$James$D$Burridge$ $ Submitted$in$Partial$Fulfillment$$ of$the$Requirements$ for$the$Degree$of$ $ Doctor$of$Philosophy$ $ December$2017$ The$dissertation$of$James$D$Burridge$was$reviewed$and$approved*$by$the$following:$ $ $ $ $ $ Jonathan$P.$Lynch$ Professor$of$Plant$Nutrition$ University$Distinguished$Professor$ Dissertation$Adviser$ Chair$of$Committee$ $ $ $ $ Kathleen$M.$Brown$ Professor$of$Plant$Stress$Biology$ ! ! ! $ Mark$J.$Guiltinan$ Professor$of$Plant$Molecular$Biology$ $ $ $ $ David$A.$Mortensen$ Professor$of$Weed$and$Applied$Plant$Ecology$ ! ! ! ! Erin$Connolly$ Professor$and$Head$of$the$Department$of$Plant$Science$ $ $ $ *Signatures$are$on$file$in$the$Graduate$School.$ ! ! $ ! ! ! $ ii$ ABSTRACT$ Grain$ legumes$ are$ important$ for$ smallTholder$ farmers$ and$ the$ socioTeconomic$ stability$of$the$world.$They$supply$proteins$to$humans$and$animals$and$contribute$ biologically$fixed$nitrogen$to$following$crops.$Low$phosphorus$(P)$availability$and$ drought$ are$ primary$ constraints$ to$ legume$ production$ in$ developing$ countries.$ Genetic$ variation$ in$ particular$ root$ architectural$ phenes$ of$ grain$ legumes$ are$ associated$ with$ improved$ acquisition$ of$ water$ and$ phosphorus.$ Quantitative$ evaluation$ of$ root$ architectural$ phenotypes$ of$ mature$ plants$ in$ the$ field$ is$ challenging.$Nonetheless,$in$situ$phenotyping$captures$responses$to$environmental$ variation$and$is$critical$to$improving$crop$performance$in$the$target$environment.$ This$ dissertation$ presents$ root$ architectural$ phenotyping$ techniques$ for$ common$ bean$ (Phaseolus) vulgaris)$ cowpea$ (Vigna) unguiculata)$ and$ several$ other$ critical$ grain$legumes.$Chapter$1$presents$the$phenotyping$techniques.$Chapter$2$connects$ cowpea$root$architecture$to$performance$through$genetic$coTlocalizations,$which$is$ a$ novel$ contribution$ for$ cowpea.$ Chapter$ 3$ presents$ results$ from$ phenotyping$ of$ other$grain$legumes,$identifies$root$architectural$patterns$in$and$among$species$and$ discusses$ opportunities$ and$ challenges$ for$ physiologists$ and$ plant$ breeders$ in$ developing$more$stress$tolerant$varieties.$$ ! ! ! ! $ iii$ ! Table!of!Contents! $ List$of$Figures$$…………………………………………….………………………………………v$ List$of$Photograph$Panels$…………………………….……………………………………..vi$$ Acknowledgments$$$…………………………….…………….……………………………….vii$ Introduction$………………………………………………….……………………………………$1$ $$$$$$$$References$$…..……………………………………….….…………………………………...5$ $ Chapter$1:$Legume$Shovelomics:$HighTThroughput$phenotyping$of$common$bean$ (Phaseolus)vulgaris$L.)$and$cowpea$(Vigna)unguiculata)subsp,$unguiculata))root$ architecture$in$the$field$$…………………………………………………………….…..……)9$ $$$$$$$$References$$$…..…………………………………………………………………………….19$ $ Chapter$2:$GenomeTwide$association$mapping$and$agronomic$impact$of$cowpea$root$ architecture$$………………………………………………………………………...….……….$21$ $$$$$$$$References$$$…..…………………………………………………………………………….31$ $ Chapter$3:$Comparative$Annual$Grain$Legume$Root$Architecture$……....$34$$$ $ $$$$$$$$References$$$….…………………………………………………………………………….50$ $$$$$$$$Figures$………………………………………………………………………………............61$ $ Epilogue$$$………………………………………………………………………………..............113$ $$$$$$$$References$$$…..…………………………………………………………………………..121$ ! ! $ iv$ LIST$OF$FIGURES$ $ Introduction$ Page$2:$Figure$1.$Common$bean$root$system$classes$from$field$example$(left)$and$ cartoon$ example$ (rigHt).$ Adventitious$ or$ Hypocotyl$ roots$ emerge$ from$ tHe$ Hypocotyl,$ basal$ roots$ emerge$ from$ tHe$ base$ of$ tHe$ Hypocotyl,$ tHe$ primary$ or$ tap$ root$is$the$radical.$ $ CHAPTER$3:$Comparative$annual$grain$legume$root$arcHitecture$$ Page$61:$Figure$1.$Drawings$depicting$differences$in$root$architecture$between$ epigeal$and$Hypogeal$germinating$species.$ Page$62:$Figure$2.$Various$legumes$on$tHe$root$system$arcHitectural$spectrum$(xT axis)$and$estimated$water$availability$in$domestication$environment$(yTaxis).$ Page$65:$Figure$3.$Violin$plot$of$branching$density$for$bean,$cowpea,$groundnut,$soy,$ tepary.$ Page$66:$Figure$4.$Violin$plot$of$BRGA$for$bean,$cowpea,$groundnut,$soy,$tepary.$ Page$67:$Figure$5.$Violin$plot$TD5$to$SD$for$bean,$chickpea,$cowpea,$groundnut,$soy,$ tepary.$ Page$68:$Figure$6.$Violin$plot$of$BRN$for$bean,$cowpea,$soy,$tepary.$ Page$69:$Figure$7.$Violin$plot$of$BRN$to$TD5$for$bean,$cowpea,$soy,$tepary.$ Page$70:$Figure$8.$Violin$plot$of$ARN$for$bean,$cowpea,$soy,$tepary.$ Page$71:$Figure$9.$Violin$plot$of$BRN$to$ARN$for$bean,$cowpea,$soy,$tepary.$ Page$72:$Figure$10.$Violin$plot$of$ARN$to$SD$for$bean,$cowpea,$soy,$tepary.$ Page$73:$Figure$11.$Violin$plot$of$BRGA$for$common$bean$gene$pools.$ Page$74:$Figure$12.$Violin$plot$of$ARN$for$common$bean$gene$pools.$ Page$75:$Figure$13.$Violin$plot$of$BRN$for$common$bean$gene$pools.$ Page$76:$Figure$14.$Violin$plot$of$TD5$for$common$bean$gene$pools.$ Page$77:$Figure$15.$Violin$plot$of$TD5$to$SD$for$common$bean$gene$pools.$ Page$78:$Figure$16.$Regression$between$TD5$and$BRN$in$Soy,$Tepary,$Cowpea$and$ Bean.$ Page$79:$Figure$17.$Regression$between$TD5$and$BRN$in$Bean.$ Page$80:$Figure$18.$Regression$between$TD5$and$BRN$plus$ARN$in$bean.$ Page$81:$Figure$19.$Regression$between$deep$and$sHallow$scores$in$groundnut,$ soybean,$tepary$bean,$cowpea$and$common$bean.$ Page$82:$Figure$20.$Regression$between$deep$and$sHallow$scores$in$common$bean.$ Page$83:$Figure$21.$Regression$between$deep$and$sHallow$scores$in$cowpea.$ Page$84:$Figure$22.$Regression$between$deep$and$sHallow$scores$in$groundnut.$ Page$85:$Figure$23.$Regression$between$deep$and$sHallow$scores$in$soybean.$ Page$86:$Figure$24.$Regression$between$deep$and$sHallow$scores$in$tepary$bean.$ Page$87:$Figure$25.$Regression$between$deep$and$sHallow$scores$in$cHickpea.$ Page$88:$Figure$26.$Violin$plot$of$sum$of$root$cross$sectional$area$relative$to$ hypocotyl$cross$sectional$area$in$bean,$cowpea,$groundnut,$soy$and$tepary.$ Page$ 89:$ Figure$ 27.$ Drawings$ depicting$ shallow,$ deep$ and$ dimorpHic$ root$ arcHitectural$pHenotypes$of$epigeal$and$Hypogeal$germinators.$ Page$90:$Table$1.$List$if$genotypes$phenotyped$by$location$and$species.$ $ v$ LIST$OF$PHOTOGRAPH$PANELS$ Chapter$3:$Comparative$annual$grain$legume$root$architecture$$ $ Page$63:$Photo$panel$1:$Representative$images$showing$variation$of$crown$root$ architecture$of$different$species.$$ Page$64:$Photo$panel$2:$Dimorphic$root$phenotypes.$ $ $ $ vi$ Acknowledgements! $ This$ research$ would$ not$ have$ been$ possible$ with$ the$ financial$ support$ and$ collaboration$of$various$foundations$and$institutions.$We$acknowledge$the$support$ of$ the$ Howard$ G$ Buffet$ Foundation,$ the$ United$ States$ Agency$ for$ International$ Development$ Global$ Hunger$ and$ Food$ Security$ Research$ Strategy:$ Climate$ Resilience,$ Nutrition,$ and$ Policy$ T$ Feed$ the$ Future$ Innovation$ Lab$ for$ Climate$ Resilience$in$Beans$Project$#$AIDTOAATAT00077,$The$McKnight$Foundation,$and$The$ Pennsylvania$State$University.$$ $ The$ findings$ and$ conclusions$ presented$ in$ this$ dissertation$ do$ not$ necessarily$ reflect$the$views$of$the$funding$agencies.$$ $ $ vii$ Introduction Root system architecture and the two resource problem Legumes are important for small-holder farmers and the socio-economic stability of the world. They supply proteins to humans and animals and contribute biologically fixed nitrogen to following crops. Common bean is the most important food legume for direct human consumption but average yield from 2011-2014 in South and Central American was 0.9 metric ton per hectare or 15% of yield potential and Sub-Saharan Africa was 0.8 metric ton per hectare or 13% of yield potential (Beaver et al., 2003; FAOSTAT, 2017). An estimated 73% of bean production is constrained by water availability and 50% by phosphorus (Beebe et al., 2009). Use of chemical fertilizers and irrigation systems are not practical for many small-holder farmers in Latin America and Sub-Sahara Africa because of lack of capital and infrastructure. Improvement of abiotic stress tolerance is critical for the food security of billions of people and legumes have the additional role of fixing nitrogen. Demand for food is estimated to increase 25%-70% by 2050 in response to a projected 9.7 billion people and increased affluence (Hunter et al., 2017; UN, 2015). Serious challenges face humanity as we face the need to achieve sustainable intensification and balance food production and environmental sustainability (Hunter et al., 2017). During this same period fertilizer will become more expensive as P becomes more scarce (Steen, 1998) and nitrogen fertilizer becomes more expensive as fuel prices rise. The situation is further compounded by challenges that are increasing in frequency and severity including; elevated temperature, altered precipitation patterns, drought, salinity, erosion, soil degradation, waterlogging, and increased cost of fertilizer (Groisman et al., 2005; St.Clair and Lynch, 2010). Varieties with superior stress tolerance must be paired with improved farming practices and cropping systems to regenerate soil and build organic matter. The precariousness of small-holder farmers and the local and regional networks they form the foundation of contributes to migration and regional instability (FAO, 2016; Maurel and Tuccio, 2016; Werz and Conley, 2012). The development and release of varieties with superior
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