Abstract
Stem mechanical strength (SMS) plays an important role in resisting stem dislodging. However, the genetic regulatory mechanisms underlying SMS in rapeseed remain unclear. In this study, a recombinant inbred line population containing 189 lines was used to investigate four SMS-related traits, namely stem breaking force (SBF), stem diameter (SD), stem weight (SW) and stem breaking strength (SBS). Accordingly, four conditional traits were also generated, namely SBF|SD, SBF|SW, SW|SD and SBS|SW. Quantitative trait locus (QTL) mapping for four unconditional SMS-related traits detected seven major QTLs, four of which were novel loci, with phenotypic contributions ranging from 10.41 to 27.22%. QTL mapping of conditional traits detected five major QTLs (including four novel loci), which explained 11.57 to 38.73% of the phenotypic variation. Comparative analyses between unconditional and conditional QTLs revealed that all 63 QTLs potentially govern biological processes (BPs) or unknown traits (UTs), which then influence SMS-related traits via 12 pathways. SBF was regulated by 13 unconditional QTLs via the QTL-BP-SD-SBF, QTL-BP-UTSD-SW-SBF, QTL-BP-SD-SW-SBF, and QTL-BP-UTSD&SW-SBF pathways, and by six conditional QTLs via the QTL-BP-SBF|SD-SBF and QTL-BP-SBF|SW-SBF pathways. SD was regulated by 18 unconditional QTLs via the QTL-BP-SD pathway, and SW by three regulatory pathways including QTL-BP-SD-SW, QTL-BP-UTSD-SW and QTL-BP-SW|SD-SW pathways. Finally, SBF potentially influences SMS via the SBF-SMS and SBF-SBS-SMS pathways. There were two additional regulatory pathways for SBS, namely QTL-BP-UTSW-SBS and QTL-BP-SBS|SW-SBS. In addition, 12 promising candidate genes were identified through multiple methods. These results contribute to our knowledge about the genetic regulatory mechanisms underlying SMS in Brassica napus.
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Abbreviations
- ANOVA:
-
Analysis of variance
- BP:
-
Biological process
- CI:
-
Confidence interval
- ICIM:
-
Inclusive composite interval mapping
- ICIM-ADD:
-
ICIM for additive QTL
- ICIM-EPI:
-
ICIM for epistatic mapping
- LOD:
-
Logarithm of odds
- PV:
-
Phenotypic variation
- QTL:
-
Quantitative trait locus
- QEI:
-
QTL by environment interaction
- SBF:
-
Stem breaking force
- SBS:
-
Stem breaking strength
- SD:
-
Stem diameter
- SMS:
-
Stem mechanical strength
- SW:
-
Stem weight
- UT:
-
Unknown trait
- UTSD :
-
Unknown trait that is highly correlated with SD
- UTSW :
-
Unknown trait that is highly correlated with SW
- UTSD and SW :
-
Unknown trait that is highly correlated with SD and SW
References
Atchley WR, Zhu J (1997) Developmental quantitative genetics, conditional epigenetic variability and growth in mice. Genetics 147:765–776
Berry PM (2013) Lodging resistance in cereals. In: Christou P, Savin R, Costa-Pierce BA, Misztal I, Whitelaw CBA (eds) Sustainable food production. Springer, New York, pp 1096–1110
Berry PM, Sterling M, Spink JH, Baker CJ, Sylvester-Bradley R, Mooney SJ, Tams AR, Ennos AR (2004) Understanding and reducing lodging in cereals. Adv Agron 84:217–271
Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19:148–162. https://doi.org/10.1105/tpc.106.044495
Bischoff V, Nita S, Neumetzler L, Schindelasch D, Urbain A, Eshed R, Persson S, Delmer D, Scheible WR (2010) TRICHOME BIREFRINGENCE and its homolog AT5G01360 encode plant-specific DUF231 proteins required for cellulose biosynthesis in Arabidopsis. Plant Physiol 153:590–602. https://doi.org/10.1104/pp.110.153320
Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295. https://doi.org/10.1105/tpc.105.031542
Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Correa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier MC, Fan G, Renault V, Bayer PE, Golicz AA, Manoli S, Lee TH, Thi VHD, Chalabi S, Hu Q, Fan C, Tollenaere R, Lu Y, Battail C, Shen J, Sidebottom CHD, Wang X, Canaguier A, Chauveau A, Berard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, Wang X, Meng J, Ma J, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury JM, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou Y, Hua W, Sharpe AG, Paterson AH, Guan C, Wincker P (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953. https://doi.org/10.1126/science.1253435
Chen F, Zhang W, Yu K, Sun L, Gao J, Zhou X, Peng Q, Fu S, Hu M, Long W, Pu H, Chen S, Wang X, Zhang J (2018) Unconditional and conditional QTL analyses of seed fatty acid composition in Brassica napus L. BMC Plant Biol 18:49. https://doi.org/10.1186/s12870-018-1268-7
Endo H, Yamaguchi M, Tamura T, Nakano Y, Nishikubo N, Yoneda A, Kato K, Kubo M, Kajita S, Katayama Y, Ohtani M, Demura T (2015) Multiple classes of transcription factors regulate the expression of VASCULAR-RELATED NAC-DOMAIN7, a master switch of xylem vessel differentiation. Plant Cell Physiol 56:242–254. https://doi.org/10.1093/pcp/pcu134
Gan Y, Liu C, Yu H, Broun P (2007) Integration of cytokinin and gibberellin signalling by Arabidopsis transcription factors GIS, ZFP8 and GIS2 in the regulation of epidermal cell fate. Development 134:2073–2081. https://doi.org/10.1242/dev.005017
Hejatko J, Ryu H, Kim GT, Dobesova R, Choi S, Choi SM, Soucek P, Horak J, Pekarova B, Palme K, Brzobohaty B, Hwang I (2009) The histidine kinases CYTOKININ-INDEPENDENT1 and ARABIDOPSIS HISTIDINE KINASE2 and 3 regulate vascular tissue development in Arabidopsis shoots. Plant Cell 21:2008–2021. https://doi.org/10.1105/tpc.109.066696
Hongo S, Sato K, Yokoyama R, Nishitani K (2012) Demethylesterification of the primary wall by PECTIN METHYLESTERASE35 provides mechanical support to the Arabidopsis stem. Plant Cell 24:2624–2634. https://doi.org/10.1105/tpc.112.099325
Hossain Z, Pillai BV, Gruber MY, Yu M, Amyot L, Hannoufa A (2018) Transcriptome profiling of Brassica napus stem sections in relation to differences in lignin content. BMC Genomics 19:255. https://doi.org/10.1186/s12864-018-4645-6
Jiang WM, Zhang DQ, Xu CX (2001) Studies on the stem anatomy of Brsssica oil to lodging. J Zhejiang Univ 27:439–442 ((in Chinese with English abstract))
Kendall SL, Holmes H, White CA, Clarke SM, Berry PM (2017) Quantifying lodging-induced yield losses in oilseed rape. Field Crop Res 211:106–113. https://doi.org/10.1016/j.fcr.2017.06.013
Ko JH, Beers EP, Han KH (2006) Global comparative transcriptome analysis identifies gene network regulating secondary xylem development in Arabidopsis thaliana. Mol Genet Genomics 276:517–531. https://doi.org/10.1007/s00438-006-0157-1
Lee Y, Choi D, Kende H (2001) Expansins: ever-expanding numbers and functions. Curr Opin Plant Biol 4:527–532. https://doi.org/10.1016/S1369-5266(00)00211-9
Li H, Ye G, Wang J (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175:361–374. https://doi.org/10.1534/genetics.106.066811
Li YC, Gu H, Qi CK (2011) Anatomical structures of root and stem of lodging resistance lines in Brassica napus L. Jiangsu J Agri Sci 27:36–44 ((in Chinese with English abstract))
Li S, Chen M, Yu D, Ren S, Sun S, Liu L, Ketelaar T, Emons AM, Liu CM (2013) EXO70A1-mediated vesicle trafficking is critical for tracheary element development in Arabidopsis. Plant Cell 25:1774–1786. https://doi.org/10.1105/tpc.113.112144
Li H, Cheng X, Zhang L, Hu J, Zhang F, Chen B, Xu K, Gao G, Li H, Li L, Huang Q, Li Z, Yan G, Wu X (2018) An integration of genome-wide association study and gene co-expression network analysis identifies candidate genes of stem lodging-related traits in Brassica napus. Front Plant Sci 9:796. https://doi.org/10.3389/fpls.2018.00796
MacMillan CP, Mansfield SD, Stachurski ZH, Evans R, Southerton SG (2010) Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus. Plant J 62(4):689–703. https://doi.org/10.1111/j.1365-313X.2010.04181.x
Meng L, Li H, Zhang L, Wang J (2015) QTL IciMapping: Integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. Crop J 3:269–283. https://doi.org/10.1016/j.cj.2015.01.001
Miller CN, Harper AL, Trick M, Wellner N, Werner P, Waldron KW, Bancroft I (2018) Dissecting the complex regulation of lodging resistance in Brassica napus. Mol Breed 38:30. https://doi.org/10.1007/s11032-018-0781-6
Ohman D, Demedts B, Kumar M, Gerber L, Gorzsas A, Goeminne G, Hedenstrom M, Ellis B, Boerjan W, Sundberg B (2013) MYB103 is required for FERULATE-5-HYDROXYLASE expression and syringyl lignin biosynthesis in Arabidopsis stems. Plant J 73:63–76. https://doi.org/10.1111/tpj.12018
Ookawa T, Hobo T, Yano M, Murata K, Ando T, Miura H, Asano K, Ochiai Y, Ikeda M, Nishitani R, Ebitani T, Ozaki H, Angeles ER, Hirasawa T, Matsuoka M (2010) New approach for rice improvement using a pleiotropic QTL gene for lodging resistance and yield. Nat Commun 1:132. https://doi.org/10.1038/ncomms1132
Rate DN, Greenberg JT (2001) The Arabidopsis aberrant growth and death2 mutant shows resistance to Pseudomonas syringae and reveals a role for NPR1 in suppressing hypersensitive cell death. Plant J 27:203–211
Sato S, Kato T, Kakegawa K, Ishii T, Liu YG, Awano T, Takabe K, Nishiyama Y, Kuga S, Sato S, Nakamura Y, Tabata S, Shibata D (2001) Role of the putative membrane-bound endo-1,4-beta-glucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol 42:251–263. https://doi.org/10.1093/pcp/pce045
Shigeto J, Kiyonaga Y, Fujita K, Kondo R, Tsutsumi Y (2013) Putative cationic cell-wall-bound peroxidase homologues in Arabidopsis, AtPrx2, AtPrx25, and AtPrx71, are involved in lignification. J Agric Food Chem 61:3781–3788. https://doi.org/10.1021/jf400426g
Tian Q, Wang X, Li C, Lu W, Yang L, Jiang Y, Luo K (2013) Functional characterization of the poplar R2R3-MYB transcription factor PtoMYB216 involved in the regulation of lignin biosynthesis during wood formation. PLoS ONE 8:e76369. https://doi.org/10.1371/journal.pone.0076369
Wang X, Yu K, Li H, Peng Q, Chen F, Zhang W, Chen S, Hu M, Zhang J (2015) High-density SNP map construction and QTL identification for the apetalous character in Brassica napus L. Front Plant Sci 6:1164. https://doi.org/10.3389/fpls.2015.01164
Wang N, Bagdassarian KS, Doherty RE, Kroon JT, Connor KA, Wang XY, Wang W, Jermyn IH, Turner SR, Etchells JP (2019) Organ-specific genetic interactions between paralogues of the PXY and ER receptor kinases enforce radial patterning in Arabidopsis vascular tissue. Dev (Cambridge, England) 146:v177105. https://doi.org/10.1242/dev.177105
Wei L, Jian H, Lu K, Yin N, Wang J, Duan X, Li W, Liu L, Xu X, Wang R, Paterson AH, Li J (2017) Genetic and transcriptomic analyses of lignin- and lodging-related traits in Brassica napus. Theor Appl Genet 130:1961–1973. https://doi.org/10.1007/s00122-017-2937-x
Wittkop B, Snowdon RJ, Friedt W (2009) Status and perspectives of breeding for enhanced yield and quality of oilseed crops for Europe. Euphytica 170:131–140. https://doi.org/10.1007/s10681-009-9940-5
Wolf S, Mouille G, Pelloux J (2009) Homogalacturonan methyl-esterification and plant development. Mol Plant 2:851–860. https://doi.org/10.1093/mp/ssp066
Wu W, Li W, Tang D, Lu H, Worland AJ (1999) Time-related mapping of quantitative trait loci underlying tiller number in rice. Genetics 151:297–303
Yan J, Zhu J, He C, Benmoussa M, Wu P (1998) Molecular dissection of developmental behavior of plant height in rice (Oryza sativa L.). Genetics 150:1257–1265
Yu K, Wang X, Chen F, Peng Q, Chen S, Li H, Zhang W, Fu S, Hu M, Long W, Chu P, Guan R, Zhang J (2018) Quantitative trait transcripts mapping coupled with expression quantitative trait loci mapping reveal the molecular network regulating the apetalous characteristic in Brassica napus L. Front Plant Sci 9:89. https://doi.org/10.3389/fpls.2018.00089
Zhao J, Becker HC, Zhang DQ, Zhang YF, Ecke W (2006) Conditional QTL mapping of oil content in rapeseed with respect to protein content and traits related to plant development and grain yield. Theor Appl Genet 113:33–38
Zhu J (1995) Analysis of conditional genetic effects and variance components in developmental genetics. Genetics 141:1633–1639
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We thank International Science Editing (http://www.internationalscienceediting.com) for editing this manuscript.
Funding
The work was supported by National Natural Science Foundation of China (31971973); the earmarked fund for China Agriculture Research System (CARS-12); Project Funded by China Postdoctoral Science Foundation (2018M630231); Open Research Fund of Key Laboratory for Biological Sciences and Genetic Improvement of Oil Crops (Ministry of Agriculture and Rural Affairs) (KF2018005); Construction Program of Biology First-class Discipline in Guizhou (GNYL[2017]009); Research Fund for Introducing Talents in Guizhou University (2018036); and Jiangsu Collaborative Innovation Center for Modern Crop Production.
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KY and WZ co-wrote the first draft of the manuscript. JZ and XW designed the project, acquired funding, and finalized the manuscript. KY and FC collected the stem segments of the AH population. KY, CS and MH investigate the phenotypic data of four SMS-related traits. YG, MZ and ET assisted and analyzed the data. All authors have reviewed and approved the final version of the manuscript and therefore are equally responsible for the integrity and accuracy of its content.
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Yu, K., Zhang, W., Guo, Y. et al. Integrating unconditional and conditional QTLs to dissect the genetic basis of stem mechanical strength in Brassica napus L. Euphytica 217, 34 (2021). https://doi.org/10.1007/s10681-021-02769-0
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DOI: https://doi.org/10.1007/s10681-021-02769-0