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Journal of Integrative Agriculture  2023, Vol. 22 Issue (11): 3394-3407    DOI: 10.1016/j.jia.2023.04.022
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Genetic dissection of crown root traits and their relationships with aboveground agronomic traits in maize

SHA Xiao-qian1*, GUAN Hong-hui2*, ZHOU Yu-qian3*, SU Er-hu4*, GUO Jian2, LI Yong-xiang2, ZHANG Deng-feng2, LIU Xu-yang2, HE Guan-hua2, LI Yu2, WANG Tian-yu2, ZOU Hua-wen1#, LI Chun-hui2#

1 College of Agriculture, Yangtze University, Jingzhou 434000, P.R.China
2 State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
3 Institute of Crops, Gansu Academy of Agricultural Sciences, Lanzhou 730070, P.R.China
4 Institute of Maize Research, Inner Mongolia Academy of Agricultural & Animal Husbandry Sciences, Hohhot 010031, P.R.China

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摘要  

冠根系统是玉米营养期和生殖期最重要的根系组成部分。然而,玉米冠根性状的遗传基础及其与地上部农艺性状的关系尚不清楚。本研究以531个玉米优良自交系为研究对象,在不同的田间环境下,对其冠根相关性状和地上部农艺性状进行表型分析。结果表明,根系性状与开花时间、株型结构、籽粒产量等地上部农艺性状呈显著正相关。通过全基因组关联分析(GWAS)结合重测序,共鉴定出115关联位点和22个高置信候选基因。其中冠根与花期和植株构型有46QTL共定位,因此大约三分之一的冠根性状遗传变异可能要归因于开花时间和植株结构。此外,115个冠根位点中有103个89.6%)位于已知的驯化和改良选择范围内,这表明冠根在玉米驯化和改良过程中可能经历了间接选择。此外,Zm00001d036901是一个高置信候选基因,其表达可能与玉米冠根的表型变异有关,Zm00001d036901在玉米驯化改良过程中是受选择的。本研究促进了我们对根系结构遗传基础的理解,并为改进玉米根系结构提供了基因组学资源。



Abstract  The crown root system is the most important root component in maize at both the vegetative and reproductive stages.  However, the genetic basis of maize crown root traits (CRT) is still unclear, and the relationship between CRT and aboveground agronomic traits in maize is poorly understood.  In this study, an association panel including 531 elite maize inbred lines was planted to phenotype the CRT and aboveground agronomic traits in different field environments.  We found that root traits were significantly and positively correlated with most aboveground agronomic traits, including flowering time, plant architecture and grain yield.  Using a genome-wide association study (GWAS) coupled with resequencing, a total of 115 associated loci and 22 high-confidence candidate genes were identified for CRT.  Approximately one-third of the genetic variation in crown root was co-located with 46 QTLs derived from flowering and plant architecture.  Furthermore, 103 (89.6%) of 115 crown root loci were located within known domestication- and/or improvement-selective sweeps, suggesting that crown roots might experience indirect selection in maize during domestication and improvement.  Furthermore, the expression of Zm00001d036901, a high-confidence candidate gene, may contribute to the phenotypic variation in maize crown roots, and Zm00001d036901 was selected during the domestication and improvement of maize.  This study promotes our understanding of the genetic basis of root architecture and provides resources for genomics-enabled improvements in maize root architecture.

Keywords:  maize        root        aboveground agronomic traits        GWAS        candidate genes  
Received: 16 November 2022   Accepted: 21 February 2023
Fund: This work was supported by grants from the National Natural Science Foundation of China (31971891), the Guangxi Key Research and Development Projects, China (GuikeAB21238004), the Scientific Innovation 2030 Project, China (2022ZD0401703), and the Modern Agro-Industry Technology Research System of Maize, China (CARS-02-03).
About author:  SHA Xiao-qian, E-mail: xq18392891030@163.com; #Correspondence ZOU Hua-wen, E-mail: zouhuawen@yangtzeu.edu.cn; LI Chun-hui, E-mail: lichunhui@caas.cn * These authors contributed equally to this study.

Cite this article: 

SHA Xiao-qian, GUAN Hong-hui, ZHOU Yu-qian, SU Er-hu, GUO Jian, LI Yong-xiang, ZHANG Deng-feng, LIU Xu-yang, HE Guan-hua, LI Yu, WANG Tian-yu, ZOU Hua-wen, LI Chun-hui. 2023. Genetic dissection of crown root traits and their relationships with aboveground agronomic traits in maize. Journal of Integrative Agriculture, 22(11): 3394-3407.

Arain S, Meer M, Sajjad M, Yasmin H. 2021. Light contributes to salt resistance through GAI protein regulation in Arabidopsis thalianaPlant Physiology and Biochemistry159, 1–11.

Asefa M, Worthy S J, Cao M, Song X, Lozano Y M, Yang J. 2022. Above- and below-ground plant traits are not consistent in response to drought and competition treatments. Annals of Botany130, 939–950.

Baez R R, Buckley Y, Yu H, Chen Z L, Gallavotti A, Nemhauser J L, Moss B L. 2020. A synthetic approach allows rapid characterization of the maize nuclear auxin response circuit. Plant Physiology182, 1713–1722.

Bjerkan K N, Grini P E. 2013. The Arabidopsis DDB1 interacting protein WDR55 is required for vegetative development. Plant Signaling & Behavior8, e25347.

Bomblies K, Doebley J F. 2006. Pleiotropic effects of the duplicate maize FLORICAULA/LEAFY genes zfl1 and zfl2 on traits under selection during maize domestication. Genetics172, 519–531.

Brown P J, Upadyayula N, Mahone G S, Tian F, Bradbury P J, Myles S, Holland J B, Flint-Garcia S, McMullen M D, Buckler E S, Rocheford T R. 2011. Distinct genetic architectures for male and female inflorescence traits of maize. PLoS Genetics7, e1002383.

Burton A L, Johnson J M, Foerster J M, Foerster J M, Hirsch C N, Buell C R, Hanlon M T, Kaeppler S M, Brown K M, Lynch J P. 2014. QTL mapping and phenotypic variation for root architectural traits in maize (Zea mays L.). Theoretical and Applied Genetics127, 2293–2311.

Cai H G, Chen F J, Mi G H, Zhang F S, Maurer H P, Liu W X, Reif J C, Yuan L X. 2012. Mapping QTLs for root system architecture of maize (Zea mays L.) in the field at different developmental stages. Theoretical and Applied Genetics125, 1313–1324.

Chen L, Li Y X, Li C H, Shi Y S, Song Y C, Zhang D F, Wang H Y, Li Y, Wang T Y. 2020. The retromer protein ZmVPS29 regulates maize kernel morphology likely through an auxin-dependent process(es). Plant Biotechnology Journal18, 1004–1014.

Chen M, Liu H, Kong J, Yang Y, Zhang N, Li R, Yue J, Huang J, Li C, Cheung A Y, Tao L Z. 2011. RopGEF7 regulates PLETHORA-dependent maintenance of the root stem cell niche in ArabidopsisPlant Cell23, 2880–2894.

Chen W K, Chen L, Zhang X, Yang N, Guo J H, Wang M, Ji S H, Zhao X Y, Yin P F, Cai L C, Xu J, Zhang L L, Han Y J, Xiao Y N, Xu G, Wang Y B, Wang S H, Wu S, Yang F, Jackson D, et al. 2022. Convergent selection of a WD40 protein that enhances grain yield in maize and rice. Science375, eabg7985.

Colombi T, Kirchgessner N, Le Marié C A, York L M, Lynch J P, Hund A. 2015. Next generation shovelomics: set up a tent and REST. Plant and Soil388, 1–20.

Dutilleul C, Ribeiro I, Blanc N, Nezames C D, Deng X W, Zglobicki P, Barrera A M P, Atehortua L, Courtois M, Labas V, Giglioli-Guivarch N, Ducos E. 2016. ASG2 is a farnesylated DWD protein that acts as ABA negative regulator in ArabidopsisPlant Cell and Environment39, 185–198.

FAO (Food and Agriculture Organization) of the United Nations Agriculture Databases. 2019. [2019-08-15]. http://www.fao.org/statistics/databases/en/

Feng X J, Jia L, Cai Y T, Guan H R, Zheng D, Zhang W X, Xiong H, Zhou H M, Wen Y, Hu Y, Zhang X M, Wang Q J, Wu F K, Xu J, Lu Y L. 2022. ABA-inducible DEEPER ROOTING 1

improves adaptation of maize to water deficiency. Plant Biotechnology Journal20, 2077–2088.

Fernández-Marco M, Desvoyes B, Manzano C, Liberman L M, Benfey P N, del Pozo J C, Gutierrez C. 2017. Control of Arabidopsis lateral root primordium boundaries by MYB36New Phytologist213, 105–112.

Gao Y Z, Lynch J P. 2016. Reduced crown root number improves water acquisition under water deficit stress in maize (Zea mays L.). Journal of Experimental Botany67, 4545–4557.

Gu D D, Mei X P, Yu T T, Sun N N, Xu D, Liu C X, Cai Y L. 2017. QTL identification for brace-root traits of maize in different generations and environments. Crop Science57, 13–21.

Hochholdinger F, Woll K, Sauer M, Dembinsky D. 2004. Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Annals of Botany93, 359–368.

Hofmann J, Hess P H, Szakasits D, Blochl A, Wieczorek K, Daxbock-Horvath S, Bohlmann H, van Bel A J E, Grundler F M W. 2009. Diversity and activity of sugar transporters in nematode-induced root syncytia. Journal of Experimental Botany60, 3085–3095.

Hufford M B, Xu X, Van Heerwaardan J, Pyhajarvi T, Chia J M, Cartwright R A, Elshire R J, Glaubitz J C, Guill K E, Kaeppler S M, Lai J, Morrell P L, Shannon L M, Song C, Springer N M, Swanson-Wagner R A, Tiffin P, Wang J, Zhang G Y, Doebley J, et al. 2012. Comparative population genomics of maize domestication and improvement. Nature Genetics44, 808–811.

Inoue T, Kondo Y, Naramoto S, Nakano A, Ueda T. 2013. RAB5 activation is required for multiple steps in Arabidopsis thaliana root development. Plant and Cell Physiology54, 1648–1659.

Ju C L, Zhang W, Liu Y, Gao Y F, Wang X F, Yan J B, Yang X H, Li J S. 2018. Genetic analysis of seedling root traits reveals the association of root trait with other agronomic traits in maize. BMC Plant Biology18, 171.

Kang H M, Sul J H, Service S K, Zaitlen N A, Kong S Y, Freimer N B, Sabatti C, Eskin E. 2010. Variance component model to account for sample structure in genome-wide association studies. Nature Genetics42, 348–354.

Kengkanna J, Jakaew P, Amawan S, Busener N, Bucksch A, Saengwilai P. 2019. Phenotypic variation of cassava root traits and their responses to drought. Applications in Plant Sciences7, e01238.

Ku L X, Sun Z H, Wang C L, Zhang J, Zhao R F, Liu H Y, Tai G Q, Chen Y H. 2012. QTL mapping and epistasis analysis of brace root traits in maize. Molecular Breeding30, 697–708.

Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T. 2005. Transcription switches for protoxylem and metaxylem vessel formation. Genes & Development19, 1855–1860.

Van Leene J, Blomme J, Kulkarni S R, Cannoot B, De Winne N, Eeckhout D, Persiau G, Van De Slijke E, Vercruysse L, Bossche R V, Heyndrickx K S, Vanneste S, Goossens A, Gevaert K, Vandepoele K, Gonzalez N, Inze D, Jaeger G D. 2016. Functional characterization of the Arabidopsis transcription factor bZIP29 reveals its role in leaf and root development. Journal of Experimental Botany67, 5825–5840.

Li C H, Guan H H, Jing X, Li Y Y, Wang B B, Li Y X, Liu X Y, Zhang D F, Liu C, Xie X Q, Zhao H Y, Wang Y B, Liu J B, Zhang P P, Hu G H, Li G L, Li S Y, Sun D Q, Wang X M, Shi Y S, et al. 2022. Genomic insights into historical improvement of heterotic groups during modern hybrid maize breeding. Nature Plants8, 750–763.

Li C H, Wang G, Zhao J L, Zhang L Q, Ai L F, Han Y F, Sun D Y, Zhang S W, Sun Y. 2014. The receptor-like kinase SIT1 mediates salt sensitivity by activating MAPK3/6 and regulating ethylene homeostasis in rice. Plant Cell26, 2538–2553.

Li P C, Fan Y Y, Yin S Y, Wang Y Y, Wang H M, Xu Y, Yang Z F, Xu C W. 2020. Multi-environment QTL mapping of crown root traits in a maize RIL population. The Crop Journal8, 645–654.

Li P C, Zhang Y Y, Yin S Y, Zhu P F, Pan T, Xu Y, Wang J Y, Hao D R, Fang H M, Xu C W, Yang Z F. 2018. QTL-by-environment interaction in the response of maize root and shoot traits to different water regimes. Frontiers in Plant Science9, 229.

Li R Y, Zeng Y J, Xu J, Wang Q, Wu F K, Cao M J, Lan H, Liu Y X, Lu Y L. 2015. Genetic variation for maize root architecture in response to drought stress at the seedling stage. Breeding Science65, 298–307.

Liang Y M, Liu Q, Wang X F, Huang C, Xu G H, Hey S, Lin H Y, Li C, Xu D Y, Wu L S, Wang C L, Wu W H, Xia J L, Xu H, Lu S J, Lai J S, Song W B, Schnable P S, Tian F. 2019. ZmMADS69 functions as a flowering activator through the ZmRap2.7-ZCN8 regulatory module and contributes to maize flowering time adaptation. New Phytologist221, 2335–2347.

Liu Q C, Deng S N, Liu B S, Tao Y F, Ai H Y, Liu J J, Zhang Y Z, Zhao Y, Xu M L. 2020. A helitron-induced RabGDI alpha variant causes quantitative recessive resistance to maize rough dwarf disease. Nature Communications11, 495.

Liu R X, Jia H T, Cao X L, Huang J, Li F, Tao Y S, Qiu F Z, Zheng Y L, Zhang Z X. 2012. Fine mapping and candidate gene prediction of a pleiotropic quantitative trait locus for yield-related trait in Zea maysPLoS ONE7, e49836.

Liu T B, Liu Q Y, Yu Z, Wang C L, Mai H F, Liu G L, Li R J, Pang G, Chen D W, Liu H L, Yang J G, Tao L Z. 2022. eIF4E1 regulates Arabidopsis embryo development and root growth by interacting with RopGEF7. Frontiers in Plant Science13, 938476.

Liu X M, An J, Han H J, Kim S H, Lim C O, Yun D J, Chung W S. 2014. ZAT11, a zinc finger transcription factor, is a negative regulator of nickel ion tolerance in ArabidopsisPlant Cell Reports33, 2015–2021.

Lynch J P. 2013. Steep, cheap and deep: An ideotype to optimize water and N acquisition by maize root systems. Annals of Botany112, 347–357.

Majer C, Xu C Z, Berendzen K W, Hochholdinger F. 2012. Molecular interactions of rootless concerning crown and seminal roots, a LOB domain protein regulating shoot–borne root initiation in maize (Zea mays L.). Philosophical Transactions of the Royal Society (B: Biological Sciences), 367, 1542–1551.

Mallika C, Waraporn T, Tatsuhito F, Stephen C, Fry J, Ketudat C. 2007. Molecular characterization of β-galactosidases from germinating rice (Oryza sativa). Plant Science173, 118–134.

Mi G H, Chen F J, Wu Q P, Lai N W, Yuan L X, Zhang F S. 2010. Ideotype root architecture for efficient nitrogen acquisition by maize in intensive cropping systems. Science China (Life Sciences), 53, 1369–1373.

Moussa A A, Mandozai A, Jin Y K, Qu J, Zhang Q, Zhao H, Anwari G, Khalifa M A S, Lamboro A, Noman M, Bakasso Y, Zhang M, Guan S Y, Wang P W. 2021. Genome-wide association screening and verification of potential genes associated with root architectural traits in maize (Zea mays L.) at multiple seedling stages. BMC Genomics22, 558.

Nibau C, Tao L Z, Levasseur K, Wu H M, Cheung A Y. 2013. The Arabidopsis small GTPase AtRAC7/ROP9 is a modulator of auxin and abscisic acid signalling. Journal of Experimental Botany64, 3425–3437.

Omori F, Mano Y. 2007. QTL mapping of root angle in F2 populations from maize ‘B73’×teosinte ‘Zea luxurians’. Plant Root1, 57–65.

Pace J, Gardner C, Romay C, Ganapathysubramanian B, Lubberstedt T. 2015. Genome-wide association analysis of seedling root development in maize (Zea mays L.). BMC Genomics16, 47.

Paez-Garcia A, Motes C M, Scheible W R, Chen R, Blancaflor E B, Monteros M J. 2015. Root traits and phenotyping strategies for plant improvement. Plants (Basel), 4, 334–355.

Ren W, Zhao L F, Liang J X, Wang L F, Chen L M, Li P C, Liu Z G, Li X J, Zhang Z H, Li J P, He K H, Zhao Z, Ail F H, Mi G H, Yan J B, Zhang F S, Chen F J, Yuan L X, Pan Q C. 2022. Genome-wide dissection of changes in maize root system architecture during modern breeding. Nature Plants8, 1408–1422.

Ribaut J M, Betran J, Monneveux P, Setter T. 2009. Drought tolerance in maize. In: Bennetzen J L, Hake S C, eds., Handbook of MaizeIts Biology. Springer Publishing, New York, USA. pp. 311–344.

Salvi S, Sponza G, Morgante M, Tomes D, Niu X, Fengler K A, Meeley R, Ananiev E V, Svitashev S, Bruggemann E, Li B, Hainey C F, Radovic S, Zaina G, Rafalski J A, Tingey S V, Miao G H, Phillips R L, Tuberosa R. 2007. Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proceedings of the National Academy of Sciences of the United States of America104, 11376–11381.

Schneider H M, Lor V S N, Hanlon M T, Perkins A, Kaepper S M, Borkar A N, Bhosale R, Zhang X, Rodriguez J, Bucksch A, Bennett M J, Brown K M, Lynch J P. 2022. Root angle in maize influences nitrogen capture and is regulated by calcineurin B-like protein (CBL)-interacting serine/threonine-protein kinase 15 (ZmCIPK15). Plant Cell and Environment45, 837–853.

Shang Q, Zhang D, Li R, Wang K, Cheng Z, Zhou Z, Hao Z, Pan J, Li X, Shi L. 2020. Mapping quantitative trait loci associated with stem-related traits in maize (Zea mays L.). Plant Molecular Biology104, 583–595.

Shen Y, Gilbert G S, Li W B, Fang M, Lu H P, Yu S X. 2019. Linking aboveground traits to root traits and local environment: Implications of the plant economics spectrum. Frontiers in Plant Science10, 1412.

Song W B, Wang B B, Hauck A L, Dong X M, Li J P, Lai J S. 2016. Genetic dissection of maize seedling root system architecture traits using an ultra-high density bin-map and a recombinant inbred line population. Journal of Integrative Plant Biology58, 266–279.

Strobl S M, Kischka D, Heilmann I, Mouille G, Schneider S. 2018. The tonoplastic inositol transporter INT1 from Arabidopsis thaliana impacts cell elongation in a sucrose-dependent way. Frontiers in Plant Science9, 1657.

Sunohara H, Kawai T, Shimizu-Sato S, Sato Y, Sato K, Kitano H. 2009. A dominant mutation of TWISTED DWARF 1 encoding an alpha-tubulin protein causes severe dwarfism and right helical growth in rice. Genes & Genetic Systems84, 209–218.

Tai H H, Lu X, Opitz N, Marcon C, Paschold A, Lithio A, Nettleton D, Hochholdinger F. 2016. Transcriptomic and anatomical complexity of primary, seminal, and crown roots highlight root type-specific functional diversity in maize (Zea mays L.). Journal of Experimental Botany67, 1123–1135.

Tian J G, Wang C L, Xia J L, Wu L S, Xu G H, Wu W H, Dan L, Qin W C, Han X, Chen Q Y, Jin W W, Tian F. 2019. Teosinte ligule allele narrows plant architecture and enhances high-density maize yields. Science365, 658–664.

Trachsel S, Kaeppler S M, Brown K M, Lynch J P. 2013. Maize root growth angles become steeper under low N conditions. Field Crops Research140, 18–31.

Vaid N, Macovei A, Tuteja N. 2013. Knights in action: Lectin receptor-like kinases in plant development and stress responses. Molecular Plant6, 1405–1418.

Vaid N, Pandey P K, Tuteja N. 2012. Genome-wide analysis of lectin receptor-like kinase family from Arabidopsis and rice. Plant Molecular Biology80, 365–388.

Wang B B, Lin Z C, Li X, Zhao Y P, Zhao B B, Wu G X, Ma X J, Wang H, Xie Y R, Li Q Q, Song G S, Kong D X, Zheng Z G, Wei H B, Shen R X, Wu H, Chen C X, Meng Z D, Wang T Y, Li Y, et al. 2020. Genome-wide selection and genetic improvement during modern maize breeding. Nature Genetics52, 565–571.

Wang F, Coe R A, Karki S, Wanchana S, Thakur V, Henry A, Lin H C, Huang J L, Peng S B, Quick W P. 2016. Overexpression of OsSAP16 regulates photosynthesis and the expression of a broad range of stress response genes in rice (Oryza sativa L.). PLoS ONE11, e0157244.

Wang H M, Tang X, Yang X Y, Fan Y Y, Xu Y, Li P C, Xu C W, Yang Z F. 2021. Exploiting natural variation in crown root traits via genome-wide association studies in maize. BMC Plant Biology21, 346.

Wang H M, Wei J, Li P C, Wang Y Y, Ge Z Z, Qian J Y, Fan Y Y, Ni J R, Xu Y, Yang Z F, Xu C W. 2019. Integrating GWAS and gene expression analysis identifies candidate genes for root morphology traits in maize at the seedling stage. Genes10, 773.

Wang X F, He F F, Ma X X, Mao C Z, Hodgman C, Lu C G, Wu P. 2011. OsCAND1 is required for crown root emergence in rice. Molecular Plant4, 289–299.

Wang Y J, Deng D X, Bian Y L, Lv Y P, Xie Q. 2010. Genome-wide analysis of primary auxin-responsive Aux/IAA gene family in maize (Zea mays L.). Molecular Biology Reports37, 3991–4001.

Woll K, Borsuk L A, Stransky H, Nettleton D, Schnable P S, Hochholdinger F. 2005. Isolation, characterization, and pericycle-specific transcriptome analyses of the novel maize lateral and seminal root initiation mutant rum1Plant Physiology139, 1255–1267.

Wu B, Ren W, Zhao L F, Li Q, Sun J Z, Chen F J, Pan Q C. 2022. Genome-wide association study of root system architecture in maize. Genes13, 181.

Wu Z C, Ren H Y, Mcgrath S P, Wu P, Zhao F J. 2011. Investigating the contribution of the phosphate transport pathway to arsenic accumulation in rice. Plant Physiology157, 498–508.

Xia R, Wang J G, Liu C Y, Wang Y, Wang Y Q, Zhai J X, Liu J, Hong X H, Cao X F, Zhu J K, Gong Z H. 2006. ROR1/RPA2A, a putative replication protein A2, functions in epigenetic gene silencing and in regulation of meristem development in ArabidopsisPlant Cell18, 85–103.

Yang X Y, Wang B C, Farris B, Clark G, Roux S J. 2015. Modulation of root skewing in Arabidopsis by apyrases and extracellular ATP. Plant and Cell Physiology56, 2197–2206.

Yazdanbakhsh N, Fisahn J. 2011. Mutations in leaf starch metabolism modulate the diurnal root growth profiles of Arabidopsis thalianaPlant Signaling & Behavior6, 995–998.

Yu X L, Wang H Y, Leung D W M, He Z D, Zhang J J, Peng X X, Liu E E. 2019. Overexpression of OsIAAGLU reveals a role for IAA-glucose conjugation in modulating rice plant architecture. Plant Cell Reports38, 731–739.

Zeng T R, Meng Z D, Yue R Q, Lu S P, Li W L, Li W C, Meng H, Sun Q. 2022. Genome wide association analysis for yield related traits in maize. BMC Plant Biology22, 449.

Zhang C, Dong S S, Xu J Y, He W M, Yang T L. 2019. PopLDdecay: A fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics35, 1786–1788.

Zhang Y X, Paschold A, Marcon C, Liu S Z, Tai H H, Nestler J, Yeh C T, Opitz N, Lanz C, Schnable P S, Hochholdinger F. 2014. The Aux/IAA gene rum1 involved in seminal and lateral root formation controls vascular patterning in maize (Zea mays L.) primary roots. Journal of Experimental Botany65, 4919–4930.

Zhang Z H, Zhang X, Lin Z L, Wang J, Xu M L, Lai J S, Yu J M, Lin Z W. 2018. The genetic architecture of nodal root number in maize. Plant Journal93, 1032–1044.

Zhong R Q, Lee C H, Ye Z H. 2010. Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. Trends in Plant Science15, 625–632.

Zhou J L, Zhong R Q, Ye Z H. 2014. Arabidopsis NAC domain proteins, VND1 to VND5, are transcriptional regulators of secondary wall biosynthesis in vessels. PLoS ONE9, e105726.

Zhu J M, Kaeppler S M, Lynch J P. 2005. Topsoil foraging and phosphorus acquisition efficiency in maize (Zea mays). Functional Plant Biology32, 749–762.

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