Quantitative trait locus analysis of adventitious and lateral root morphology of barley grown at low and high P
Jingyi Guo A * , Guangdeng Chen A * , Xizhou Zhang A C , Tingxuan Li A , Haiying Yu A and Chunji Liu B
+ Author Affiliations
- Author Affiliations
A College of Resources, Sichuan Agricultural University, Chengdu 611130, China.
B CSIRO Agriculture, 306 Carmody Road, St Lucia, Qld 4067, Australia.
C Corresponding author. Email: zhangxzhou@126.com
Functional Plant Biology 45(9) 957-967 https://doi.org/10.1071/FP17271
Submitted: 28 September 2017 Accepted: 15 March 2018 Published: 12 April 2018
Abstract
Barley (Hordeum vulgare L) may alter its root morphology to improve P acquisition efficiency under low-P (LP) stress. This research studied the variations in adventitious and lateral root morphological traits of barley and mapped their quantitative trait loci (QTLs) under LP and high P (HP). The recombinant inbred lines were derived from the F1 population of a cross between CN4027 and Baudin. Two experiments aimed to identify QTLs related to adventitious and lateral root morphological traits under LP and HP. The length, surface area and volume of adventitious and lateral roots were measured. Under HP, Baudin had larger root morphology, especially lateral root morphology, than CN4027. LP stress induced lateral root growth but inhibited adventitious root growth. Nineteen QTLs for root morphological traits were detected. These QTLs clustered within four regions (Cl−2H, Cl−3H, Cl−4H and Cl−7H) on chromosomes 2H, 3H, 4H and 7H, with corresponding contributions of 12.0–42.9%. Some QTLs are linked with the QTLs for P efficiency detected previously, demonstrating the role of root morphological traits in P efficiency. The Cl−2H region was identified in the interval bPb3927665–bPb3265744 on chromosome 2H and had major effects on lateral root growth, especially under LP. Lateral root length and surface area increased when alleles from Baudin were present at the QTLs in Cl−2H. This study demonstrated the patterns of growth among root types and the role of lateral roots in barley’s adaption to LP stress. The QTL clusters, especially Cl−2H, may offer clues for fine mapping and map-based cloning.
Additional keywords: Hordeum vulgare L., phosphate deficiency, root growth.
References
Bai C, Liang Y, Hawkesford MJ (2013) Identification of QTLs associated with seedling root traits and their correlation with plant height in wheat. Journal of Experimental Botany 64, 1745–1753.| Identification of QTLs associated with seedling root traits and their correlation with plant height in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsV2ktrc%3D&md5=3ef3794b4c993978106f71edcc378e58CAS |
Bates TR, Lynch JP (2000) Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae). American Journal of Botany 87, 958–963.
| Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvVemsb0%3D&md5=107687ef347cac3007b867c38aca0180CAS |
Beebe SE, Rojas-Pierce M, Yan X, Blair MW, Pedraza F, Muñoz F, Tohme J, Lynch JP (2006) Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Science 46, 413–423.
| Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFKjsbk%3D&md5=bcb552ecaec72ca2f2a9671d838e68dfCAS |
Bhadoria PS, Dessougi HE, Liebersbach H, Claassen N (2004) Phosphorus uptake kinetics, size of root system and growth of maize and groundnut in solution culture. Plant and Soil 262, 327–336.
| Phosphorus uptake kinetics, size of root system and growth of maize and groundnut in solution culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtlGgu7k%3D&md5=39fa56cbea1379986dff89b8ab256f57CAS |
Courtois B, Ahmadi N, Khowaja F, Price AH, Rami J-F, Frouin J, Hamelin C, Ruiz M (2009) Rice root genetic architecture: meta-analysis from a drought QTL database. Rice (New York, N.Y.) 2, 115–128.
| Rice root genetic architecture: meta-analysis from a drought QTL database.Crossref | GoogleScholarGoogle Scholar |
de Dorlodot S, Forster B, Pagès L, Price A, Tuberosa R, Draye X (2007) Root system architecture: opportunities and constraints for genetic improvement of crops. Trends in Plant Science 12, 474–481.
| Root system architecture: opportunities and constraints for genetic improvement of crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFWgsLjP&md5=4136fb3f184c11dac2c2c5668fc6c569CAS |
Ding Z, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proceedings of the National Academy of Sciences of the United States of America 107, 12046–12051.
| Auxin regulates distal stem cell differentiation in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVartbk%3D&md5=492a087ae60575bb0ab019e5f475bb4cCAS |
Duan L, Dietrich D, Ng CH, Chan PMY, Bhalerao R, Bennett MJ, Dinneny JR (2013) Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. The Plant Cell 25, 324–341.
| Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntVCktrY%3D&md5=0a2988c98a0a8d6af01e565cd07977f3CAS |
Gahoonia TS, Nielsen NE (1997) Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98, 177–182.
| Variation in root hairs of barley cultivars doubled soil phosphorus uptake.Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS, Nielsen NE (2003) Phosphorus (P) uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low‐and high‐P soils. Plant, Cell & Environment 26, 1759–1766.
| Phosphorus (P) uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low‐and high‐P soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptlaht7c%3D&md5=a848eacf673c67a4f69bb70da3238347CAS |
Gahoonia TS, Nielsen NE (2004) Root traits as tools for creating phosphorus efficient crop varieties. Plant and Soil 260, 47–57.
| Root traits as tools for creating phosphorus efficient crop varieties.Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS, Care D, Nielsen NE (1997) Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant and Soil 191, 181–188.
| Root hairs and phosphorus acquisition of wheat and barley cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmt1Kks7s%3D&md5=817b263b9b2d16033c0234fe267fd8c8CAS |
Gahoonia TS, Nielsen NE, Joshi PA, Jahoor A (2001) A root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake. Plant and Soil 235, 211–219.
| A root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotFahurg%3D&md5=e7ad42f17905ce8c01f73402173bae75CAS |
Gao S, Chen G, Hu D, Zhang X, Li T, Liu S, Liu C (2017) A major quantitative trait locus controlling phosphorus utilization effciency under different phytate-P conditions at vegetative stage in barley. Journal of Integrative Agriculture 16, 60345–60347.
George TS, Brown LK, Ramsay L, White PJ, Newton AC, Bengough AG, Russell J, Thomas WT (2014) Understanding the genetic control and physiological traits associated with rhizosheath production by barley (Hordeum vulgare). New Phytologist 203, 195–205.
| Understanding the genetic control and physiological traits associated with rhizosheath production by barley (Hordeum vulgare).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXovFWkt7Y%3D&md5=c4b3d0eb94dfc43c3cee22a12dcbe528CAS |
Gilbert GA, Knight JD, Vance CP, Allan DL (2000) Proteoid root development of phosphorus deficient lupin is mimicked by auxin and phosphonate. Annals of Botany 85, 921–928.
| Proteoid root development of phosphorus deficient lupin is mimicked by auxin and phosphonate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjs12hu70%3D&md5=8470116f9571839cc96ff2579b41f183CAS |
Gong X, McDonald G (2017) QTL mapping of root traits in phosphorus-deficient soils reveals important genomic regions for improving NDVI and grain yield in barley. Theoretical and Applied Genetics 130, 1885–1902.
| QTL mapping of root traits in phosphorus-deficient soils reveals important genomic regions for improving NDVI and grain yield in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtVKitL7J&md5=54d59d0a9bbbd55ca2923b1440108479CAS |
Gong X, Wheeler R, Bovill WD, McDonald GK (2016) QTL mapping of grain yield and phosphorus efficiency in barley in a Mediterranean-like environment. Theoretical and Applied Genetics 129, 1657–1672.
| QTL mapping of grain yield and phosphorus efficiency in barley in a Mediterranean-like environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XotF2lu7w%3D&md5=c8f9157fd9e04964ad9c7369ea203118CAS |
Gu R, Chen F, Long L, Cai H, Liu Z (2016) Enhancing phosphorus uptake efficiency through QTL-based selection for root system architecture in maize. Journal of Genetics and Genomics 43, 663–672.
| Enhancing phosphorus uptake efficiency through QTL-based selection for root system architecture in maize.Crossref | GoogleScholarGoogle Scholar |
Guo J, Chen G, Zhang X, Li T, Yu H, Chen H (2017) Mapping quantitative trait loci for tolerance to phosphorus-deficiency at the seedling stage in barley. Euphytica 213, 114
| Mapping quantitative trait loci for tolerance to phosphorus-deficiency at the seedling stage in barley.Crossref | GoogleScholarGoogle Scholar |
Ho MD, Rosas JC, Brown KM, Lynch JP (2005) Root architectural tradeoffs for water and phosphorus acquisition. Functional Plant Biology 32, 737–748.
| Root architectural tradeoffs for water and phosphorus acquisition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvVOgsLw%3D&md5=2d4bf0a0208286f186560a84747f6740CAS |
Hoffmann A, Maurer A, Pillen K (2012) Detection of nitrogen deficiency QTL in juvenile wild barley introgression lines growing in a hydroponic system. BMC Genetics 13, 88
| Detection of nitrogen deficiency QTL in juvenile wild barley introgression lines growing in a hydroponic system.Crossref | GoogleScholarGoogle Scholar |
Islamovic E, Obert DE, Oliver RE (2013) A new genetic linkage map of barley (Hordeum vulgare L.) facilitates genetic dissection of height and spike length and angle. Field Crops Research 154, 91–99.
| A new genetic linkage map of barley (Hordeum vulgare L.) facilitates genetic dissection of height and spike length and angle.Crossref | GoogleScholarGoogle Scholar |
Li J, Xie Y, Dai A, Liu L, Li Z (2009) Root and shoot traits responses to phosphorus deficiency and QTL analysis at seedling stage using introgression lines of rice. Journal of Genetics and Genomics 36, 173–183.
| Root and shoot traits responses to phosphorus deficiency and QTL analysis at seedling stage using introgression lines of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVOrsL4%3D&md5=2b8d509bd7be35b163d6e3735ff46bcaCAS |
Li P, Chen F, Cai H, Liu J, Pan Q, Liu Z, Gu R, Mi G, Zhang F, Yuan L (2015) A genetic relationship between nitrogen use efficiency and seedling root traits in maize as revealed by QTL analysis. Journal of Experimental Botany 66, 3175–3188.
| A genetic relationship between nitrogen use efficiency and seedling root traits in maize as revealed by QTL analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVCqu7vP&md5=96866592bc9484d06d8642c37bc12ae5CAS |
Liang Q, Cheng X, Mei M, Yan X, Liao H (2010) QTL analysis of root traits as related to phosphorus efficiency in soybean. Annals of Botany 106, 223–234.
| QTL analysis of root traits as related to phosphorus efficiency in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVWjsb0%3D&md5=be91bcd85f7e1c16a5354887d477b11eCAS |
Liao MT, Hocking PJ, Dong B, Delhaize E, Richardson AE, Ryan PR (2008) Variation in early phosphorus-uptake efficiency among wheat genotypes grown on two contrasting Australian soils. Crop and Pasture Science 59, 157–166.
| Variation in early phosphorus-uptake efficiency among wheat genotypes grown on two contrasting Australian soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVGhsbg%3D&md5=b4819d3b1e9613b7b449065da2c87e7fCAS |
Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiology 156, 1041–1049.
| Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFWlurY%3D&md5=565575e29abe6d285dc443f908f26f34CAS |
Ma Z, Thomas CW, Marcus A, Lynch JP (2001) Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: a modeling approach. Plant and Soil 236, 221–235.
| Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: a modeling approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptlKhu74%3D&md5=cc143d4a7fec8a29b4a134497625d921CAS |
Mehrvarz S, Chaichi MR, Alikhani HA (2008) Effect of phosphate solubilizing microorganisms and phosphorus chemical fertilizer on forage and grain quality of barely (Hordeum vulgare L.). American-Eurasian Journal of Agricultural & Environmental Sciences. 3, 855–860.
Naz AA, Arifuzzaman M, Muzammil S, Pillen K, Léon J (2014) Wild barley introgression lines revealed novel QTL alleles for root and related shoot traits in the cultivated barley (Hordeum vulgare L.). BMC Genetics 15, 107
| Wild barley introgression lines revealed novel QTL alleles for root and related shoot traits in the cultivated barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar |
Negi S, Sukumar P, Liu X, Cohen JD, Muday GK (2010) Genetic dissection of the role of ethylene in regulating auxin‐dependent lateral and adventitious root formation in tomato. The Plant Journal 61, 3–15.
| Genetic dissection of the role of ethylene in regulating auxin‐dependent lateral and adventitious root formation in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovF2lsw%3D%3D&md5=8dfc1552d437f90224db521f74687443CAS |
Ochoa IE, Blair MW, Lynch JP (2006) QTL analysis of adventitious root formation in common bean under contrasting phosphorus availability. Crop Science 46, 1609–1621.
| QTL analysis of adventitious root formation in common bean under contrasting phosphorus availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotV2jurg%3D&md5=0879f120f4791edcf9bcc6f4bd58a806CAS |
Péret B, Clément M, Nussaume L, Desnos T (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends in Plant Science 16, 442–450.
| Root developmental adaptation to phosphate starvation: better safe than sorry.Crossref | GoogleScholarGoogle Scholar |
Ramaekers L, Remans R, Rao IM, Blair MW, Vanderleyden J (2010) Strategies for improving phosphorus acquisition efficiency of crop plants. Field Crops Research 117, 169–176.
| Strategies for improving phosphorus acquisition efficiency of crop plants.Crossref | GoogleScholarGoogle Scholar |
Ren Y, He X, Liu D, Li J, Zhao X, Li B, Tong Y, Zhang A, Li Z (2012) Major quantitative trait loci for seminal root morphology of wheat seedlings. Molecular Breeding 30, 139–148.
| Major quantitative trait loci for seminal root morphology of wheat seedlings.Crossref | GoogleScholarGoogle Scholar |
Rose TJ, Impa SM, Rose MT, Pariasca-Tanaka J, Mori A, Heuer S, Johnson-Beebout SE, Wissuwa M (2013) Enhancing phosphorus and zinc acquisition efficiency in rice: a critical review of root traits and their potential utility in rice breeding. Annals of Botany 112, 331–345.
| Enhancing phosphorus and zinc acquisition efficiency in rice: a critical review of root traits and their potential utility in rice breeding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSiur%2FM&md5=f57077e26f1c2ea53fcae8c29386b5a7CAS |
Rosquete MR, Wangenheim DV, Marhavý P, Barbez E, Stelzer EHK, Benková E, Maizel A, Kleine-Vehn J (2013) An auxin transport mechanism restricts positive orthogravitropism in lateral roots. Current Biology 23, 817–822.
| An auxin transport mechanism restricts positive orthogravitropism in lateral roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvVWht7k%3D&md5=dbb2023cc221ec750c29565806472107CAS |
Sharma S, Xu S, Ehdaie B, Hoops A, Close TJ, Lukaszewski AJ, Waines JG (2011) Dissection of QTL effects for root traits using a chromosome arm-specific mapping population in bread wheat. Theoretical and Applied Genetics 122, 759–769.
| Dissection of QTL effects for root traits using a chromosome arm-specific mapping population in bread wheat.Crossref | GoogleScholarGoogle Scholar |
Shen J, Li H, Neumann G, Zhang F (2005) Nutrient uptake, cluster root formation and exudation of protons and citratein Lupinus albusas affected by localized supply of phosphorus in a split-root system. Plant Science 168, 837–845.
| Nutrient uptake, cluster root formation and exudation of protons and citratein Lupinus albusas affected by localized supply of phosphorus in a split-root system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXosVGgsQ%3D%3D&md5=5a7ac40625f6e36be6a827b188181106CAS |
Shimizu A, Yanagihara S, Kawasaki S, Ikehashi H (2004) Phosphorus deficiency-induced root elongation and its QTL in rice (Oryza sativa L.). Theoretical and Applied Genetics 109, 1361–1368.
| Phosphorus deficiency-induced root elongation and its QTL in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVahur7L&md5=0a3c3877e365b80a99fb90601d11dfd0CAS |
Steingrobe B (2001) Root renewal of sugar beet as a mechanism of P uptake efficiency. Journal of Plant Nutrition and Soil Science 164, 533–539.
| Root renewal of sugar beet as a mechanism of P uptake efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvF2gt70%3D&md5=dcdf888155546b23974d641340a89cdcCAS |
Tian H, De Smet I, Ding Z (2014) Shaping a root system: regulating lateral versus primary root growth. Trends in Plant Science 19, 426–431.
| Shaping a root system: regulating lateral versus primary root growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitlChs7k%3D&md5=2a2d9e524f4fb9aa73dbdb3531c453f8CAS |
Van Ooijen JW (2004) ‘MapQTL version 5.0. Software for the mapping of quantitative trait loci in experimental populations.’ (Kyazma BV: Wageningen)
Voorrips RE (2002) MAPCHART: software for the graphical presentation of linkage maps and QTLs. The Journal of Heredity 93, 77–78.
| MAPCHART: software for the graphical presentation of linkage maps and QTLs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlOntrw%3D&md5=b97061403794603f4390848f14294ec1CAS |
Wang B, Shen J, Tang C, Rengel Z (2008) Root morphology, proton release, and carboxylate exudation in lupin in response to phosphorus deficiency. Journal of Plant Nutrition 31, 557–570.
| Root morphology, proton release, and carboxylate exudation in lupin in response to phosphorus deficiency.Crossref | GoogleScholarGoogle Scholar |
Wang X, Shen J, Liao H (2010) Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops? Plant Science 179, 302–306.
| Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvFKkur0%3D&md5=6a3c9a740f74572e1601432ca6b95402CAS |
Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiology 126, 875–882.
| Phosphate availability regulates root system architecture in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXks1GmsLs%3D&md5=678421cce4b4de3d86e7e38b0b3d6fc4CAS |
Wissuwa M, Ae N (2001) Further characterization of two QTLs that increase phosphorus uptake of rice (Oryza sativa L.) under phosphorus deficiency. Plant and Soil 237, 275–286.
| Further characterization of two QTLs that increase phosphorus uptake of rice (Oryza sativa L.) under phosphorus deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVWksw%3D%3D&md5=dae1fb210208a956a095df8578c60adfCAS |
Yan X, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant and Soil 265, 17–29.
| QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXns12ltg%3D%3D&md5=f32f113f8a83cd46b7c23a3b9f79fdaaCAS |
Yang M, Ding G, Shi L, Feng J, Xu F, Meng J (2010) Quantitative trait loci for root morphology in response to low phosphorus stress in Brassica napus. Theoretical and Applied Genetics 121, 181–193.
| Quantitative trait loci for root morphology in response to low phosphorus stress in Brassica napus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFagu7Y%3D&md5=d670e8534fc9c09debb30e12a05d144aCAS |
Yang M, Ding G, Shi L, Xu F, Meng J (2011) Detection of QTL for phosphorus efficiency at vegetative stage in Brassica napus. Plant and Soil 339, 97–111.
| Detection of QTL for phosphorus efficiency at vegetative stage in Brassica napus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVCguw%3D%3D&md5=997ddeaaeacd5fe347366caefa602763CAS |
Yuan Y, Gao M, Zhang M, Zheng H, Zhou X, Guo Y, Zhao Y, Kong F, Li S (2017) QTL mapping for phosphorus efficiency and morphological traits at seedling and maturity stages in wheat. Frontiers in Plant Science 8, 614
| QTL mapping for phosphorus efficiency and morphological traits at seedling and maturity stages in wheat.Crossref | GoogleScholarGoogle Scholar |
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Research 14, 415–421.
| A decimal code for the growth stages of cereals.Crossref | GoogleScholarGoogle Scholar |
Zhu J, Lynch JP (2004) The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings. Functional Plant Biology 31, 949–958.
| The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXosFSqu7k%3D&md5=271512131c96b8eb746a12dab4ed4549CAS |
Zhu J, Kaeppler SM, Lynch JP (2005) Mapping of QTLs for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply. Theoretical and Applied Genetics 111, 688–695.
| Mapping of QTLs for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXos1GjsLg%3D&md5=6c4d7352f9a80f12a49b830dc4f363b3CAS |
Zhu J, Mickelson SM, Kaeppler SM, Lynch JP (2006) Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels. Theoretical and Applied Genetics 113, 1–10.
| Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvVGru74%3D&md5=f9d4fcab1835fde99e989b618dbab9abCAS |
