Variation for heterodimerization and nuclear localization among known and novel oil palm SHELL alleles.
tenera
Elaeis guineensis (oil palm)
MADS-box genes
SHELL
heterosis
oil yield
subcellular localization
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
16
08
2019
accepted:
06
12
2019
pubmed:
22
12
2019
medline:
15
5
2021
entrez:
22
12
2019
Statut:
ppublish
Résumé
Oil palm breeding involves crossing dura and pisifera palms to produce tenera progeny with greatly improved oil yield. Oil yield is controlled by variant alleles of a type II MADS-box gene, SHELL, that impact the presence and thickness of the endocarp, or shell, surrounding the fruit kernel. We identified six novel SHELL alleles in noncommercial African germplasm populations from the Malaysian Palm Oil Board. These populations provide extensive diversity to harness genetic, mechanistic and phenotypic variation associated with oil yield in a globally critical crop. We investigated phenotypes in heteroallelic combinations, as well as SHELL heterodimerization and subcellular localization by yeast two-hybrid, bimolecular fluorescence complementation and gene expression analyses. Four novel SHELL alleles were associated with fruit form phenotype. Candidate heterodimerization partners were identified, and interactions with EgSEP3 and subcellular localization were SHELL allele-specific. Our findings reveal allele-specific mechanisms by which variant SHELL alleles impact yield, as well as speculative insights into the potential role of SHELL in single-gene oil yield heterosis. Future field trials for combinability and introgression may further optimize yield and improve sustainability.
Substances chimiques
Palm Oil
5QUO05548Z
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
426-440Informations de copyright
© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.
Références
Battaglia R, Brambilla V, Colombo L, Stuitje AR, Kater MM. 2006. Functional analysis of MADS-box genes controlling ovule development in Arabidopsis using the ethanol-inducible alc gene-expression system. Mechanisms of Development 123: 267-276.
Beirnaert A, Vanderweyen R. 1941. Contribution a l'etude genetique et biometrique des varieties d'Elaeis guineensis Jacquin. Publications de l'Institut National Pour l'Etude Agronomic du Congo Belge. Série Scientifique 27: 1-101.
Birchler JA. 2015. Heterosis: the genetic basis of hybrid vigour. Nature Plants 1: 15020.
Birchler JA, Yao H, Chudalayandi S, Vaiman D, Veitia RA. 2010. Heterosis. Plant Cell 22: 2105-2112.
Bray NL, Pimentel H, Melsted P, Pachter L. 2016. Near-optimal probabilistic RNA-seq quantification. Nature Biotechnology 34: 525-527.
Chida K, Nagamori S, Kuroki T. 1999. Nuclear translocation of Fos is stimulated by interaction with Jun through the leucine zipper. Cellular and Molecular Life Sciences 55: 297-302.
Corley RHV, Lee CH. 1992. The physiological basis for genetic improvement of oil palm in Malaysia. Euphytica 60: 179-184.
Corley RHV, Tinker PB. 2007. The oil palm. Oxford, UK: Blackwell Science.
Cui R, Han J, Zhao S, Su K, Wu F, Du X, Xu Q, Chong K, Theissen G, Meng Z. 2010. Functional conservation and diversification of class E floral homeotic genes in rice (Oryza sativa). The Plant Journal 61: 767-781.
Darwin CR. 1876. The effects of cross and self fertilisation in the vegetable kingdom. London, UK: John Murray.
de Folter S, Immink RG, Kieffer M, Parenicová L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM et al. 2005. Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 17: 1424-1433.
Delneri D, Hoyle DC, Gkargkas K, Cross EJ, Rash B, Zeef L, Leong HS, Davey HM, Hayes A, Kell DB et al. 2008. Identification and characterization of high-flux-control genes of yeast through competition analyses in continuous cultures. Nature Genetics 40: 113-117.
Dingwall C, Laskey RA. 1991. Nuclear targeting sequences-a consensus? Trends in Biochemical Sciences 16: 478-481.
Dinneny JR, Yanofsky MF. 2005. Drawing lines and borders: how the dehiscent fruit of Arabidopsis is patterned. Bioessays 27: 42-49.
Dollinger EJ. 1985. Effects of visible recessive alleles on vigor characteristics in a maize hybrid. Crop Science 25: 819-821.
Dreni L, Jacchia S, Fornara F, Fornari M, Ouwerkerk PB, An G, Colombo L, Kater MM. 2007. The D-lineage MADS-box gene OsMADS13 controls ovule identity in rice. The Plant Journal 52: 690-699.
East EM. 1936. Heterosis. Genetics 21: 375-397.
Favaro R, Pinyopich A, Battaglia R, Kooiker M, Borghi L, Ditta G, Yanofsky MF, Kater MM, Colombo L. 2003. MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15: 2603-2611.
Ferrario S, Shchennikova AV, Franken J, Immink RG, Angenent GC. 2006. Control of floral meristem determinacy in petunia by MADS-box transcription factors. Plant Physiology 140: 890-898.
Fievet JB, Nidelet T, Dillman C, de Vienne D. 2018. Heterosis is a systemic property emerging from non-linear genotype-phenotype relationships: evidence from in vitro genetics and computer simulations. Frontiers in Genetics 9: 159.
Gascon JP, Wuidart W. 1975. Amelioration de la production et de la qualite de l'huile d'Elaeis guineensis Jacq. Oleagineux 30: 1-4.
Gustafson FG. 1946. Influence of external and internal factors on growth hormone in green plants. Plant Physiology 21: 49-62.
Hartley CWS. 1988. The oil palm. London, UK: Longman.
Hu CD, Chinenov Y, Kerppola TK. 2002. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Molecular Cell 9: 789-798.
Huang H, Tudor M, Su T, Zhang Y, Hu Y, Ma H. 1996. DNA binding properties of two Arabidopsis MADS domain proteins: binding consensus and dimer formation. Plant Cell 8: 81-94.
Humle T, Matsuzawa T. 2004. Oil palm use by adjacent communities of chimpanzees at Bossou and Nimba Mountains, West Africa. International Journal of Primatology 25: 551-581.
Immink RG, Gadella TW, Ferrario S, Busscher M, Angenent GC. 2002. Analysis of MADS box protein-protein interactions in living plant cells. Proceedings of the National Academy of Sciences, USA 99: 2416-2421.
Immink RG, Kaufmann K, Angenent GC. 2010. The ‘ABC’ of MADS domain protein behaviour and interactions. Seminars in Cell and Developmental Biology 21: 87-93.
Immink RG, Tonaco IA, de Folter S, Shchennikova A, van Dijk AD, Busscher-Lange J, Borst JW, Angenent GC. 2009. SEPALLATA3: the ‘glue’ for MADS box transcription factor complex formation. Genome Biology 10: R24.
Jin J, Sun Y, Qu J, Syah R, Lim CH, Alfiko Y, Rahman NEB, Suwanto A, Yue G, Wong L et al. 2017. Transcriptome and functional analysis reveals hybrid vigor for oil biosynthesis in oil palm. Scientific Reports 7: 439.
Kosugi S, Hasebe M, Matsumura N, Takashima H, Miyamoto-Sato E, Tomita M, Yanagawa H. 2009. Six classes of nuclear localization signals specific to different binding grooves of importin α. Journal of Biological Chemistry 284: 478-485.
Krieger U, Lippman ZB, Zamir D. 2010. The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nature Genetics 42: 459-463.
Kushairi A, Loh SK, Azman I, Hishamuddin E, Ong-Abdullah M, Izuddin MZBMN, Razmah G, Sundram S, Parveez GKA. 2018. Oil palm economic performance in Malaysia and R&D progress in 2017. Journal of Oil Palm Research 30: 163-195.
Lee YL, Fang MJ, Kuang LY, Gelvin SB. 2008. Vectors for multi-color bimolecular fluorescence complementation to investigate protein-protein interactions in living plant cells. Plant Methods 4: 24.
Lee LY, Gelvin SB. 2014. Bimolecular fluorescence complementation for imaging protein interactions in plant hosts of microbial pathogens. Methods in Molecular Biology 1197: 185-208.
Li H, Li J, Song J, Zhao B, Guo C, Wang B, Zhang Q, Wang J, King GJ, Liu K. 2019. An auxin signaling gene BnaA3.IAA7 contributes to improved plant architecture and yield heterosis in rapeseed. New Phytologist 222: 837-851.
Li H, Yang Q, Gao L, Zhang M, Ni X, Zhang Y. 2017. Identification of heterosis-associated stable QTLs for ear-weight-related traits in an elite maize hybrid Zhengdan 958 by Design III. Frontiers in Plant Science 8: 561.
Liu C, Zhang J, Zhang N, Shan H, Su K, Meng Z, Kong H, Chen Z. 2010. Interactions among proteins of floral MADS-box genes in basal eudicots: implications for evolution of the regulatory network for flower development. Molecular Biology and Evolution 27: 1598-1611.
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15: 550.
McGonigle B, Bouhidel K, Irish VF. 1996. Nuclear localization of the Arabidopsis APETALA3 and PISTILLATA homeotic gene products depends on their simultaneous expression. Genes & Development 10: 1812-1821.
Moore S, Lukens L. 2011. An evaluation of Arabidopsis thaliana hybrid traits and their genetic control. G3 1: 571-579.
Nagoshi E, Yoneda Y. 2001. Dimerization of sterol regulatory element-binding protein 2 via the helix-loop-helix-leucine zipper domain is a prerequisite for its nuclear localization mediated by importin β. Molecular and Cellular Biology 21: 2779-2789.
OIL WORLD. 2017. Oil world statistics update, 17 oil and fats: World summary balances. Hamburg, Germany: ISTA Mielke.
Ooi LCL, Low ETL, Ong-Abdullah M, Nookiah R, Ting NC, Nagappan J, Manaf MAA, Chan KL, Halim MA, Azizi N et al. 2016. Non-tenera contamination and the economic impact of SHELL genetic testing in the Malaysian independent oil palm industry. Frontiers in Plant Science 7: 771.
Pellegrini L, Tan S, Richmond TJ. 1995. Structure of serum response factor core bound to DNA. Nature 376: 490-498.
Price Z, Mayes S, Billotte N, Hafeez N, Dumortier F, MacDonald D. 2007. Oil Palm. Genome mapping and molecular breeding in plants. Volume 6: Technical crops. Heidelberg, Germany: Springer-Verlag.
Rajanaidu N. 1997. Exploitation of heterosis in oil palm to increase oil yield. Book of abstracts. International Symposium - The genetics and exploitation of heterosis in Crops. Mexico City, Mexico.
Rajanaidu N, Kushairi A, Mohd Din A. 2017. Utilization of germplasm. Bangi, Malaysia: Monograph Oil Palm Genetic Resources.
Richards E, Reichardt M, Rogers S. 1994. Preparation of genomic DNA from plant tissue. Current Protocols in Molecular Biology 27: 2.3.1-2.3.7.
Robbins J, Dilworth SM, Laskey RA, Dingwall C. 1991. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64: 615-623.
Rédei GP. 1962. Supervital mutants of Arabidopsis. Genetics 47: 443-460.
Schnable PS, Springer NM. 2013. Progress toward understanding heterosis in crop plants. Annual Review of Plant Biology 64: 71-88.
Singh R, Low ETL, Ooi LC, Ong-Abdullah M, Ting NC, Nagappan J, Nookiah R, Amiruddin MD, Rosli R, Manaf MA et al. 2013a. The oil palm SHELL gene controls oil yield and encodes a homologue of SEEDSTICK. Nature 500: 340-344.
Singh R, Ong-Abdullah M, Low ETL, Manaf MA, Rosli R, Nookiah R, Ooi LC, Ooi SE, Chan KL, Halim MA et al. 2013b. Oil palm genome sequence reveals divergence of interfertile species in Old and New worlds. Nature 500: 335-339.
Spit A, Hyland RH, Mellor EJ, Casselton LA. 1998. A role for heterodimerization in nuclear localization of a homeodomain protein. Proceedings of the National Academy of Sciences, USA 95: 6228-6233.
Teh CK, Muaz SD, Tangaya P, Fong PY, Ong AL, Mayes S, Chew FT, Kulaveerasingam H, Appleton D. 2017. Characterizing haploinsufficiency of SHELL gene to improve fruit form prediction in introgressive hybrids of oil palm. Scientific Reports 7: 3118.
Veitia RA. 2010. A generalized model of gene dosage and dominant negative effects in macromolecular complexes. FASEB Journal 24: 994-1002.
Veitia RA, Vaiman D. 2011. Exploring the mechanistic bases of heterosis from the perspective of macromolecular complexes. FASEB Journal 25: 476-482.