Expression of key auxin biosynthesis genes correlates with auxin and starch content of developing wheat (Triticum aestivum) grains
Muhammed Rezwan Kabir A , Heather M. Nonhebel A C , David Backhouse B and Gal Winter AA School of Science and Technology, University of New England, Armidale, NSW 2351, Australia.
B School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.
C Corresponding author. Email: hnonheb2@une.edu.au
Functional Plant Biology 48(8) 802-814 https://doi.org/10.1071/FP20319
Submitted: 13 October 2020 Accepted: 23 February 2021 Published: 15 March 2021
Abstract
The effect of auxin on wheat (Triticum aestivum L.) grain size is contentious. Additionally, the contributions to the IAA pool from de novo synthesis versus hydrolysis of IAA-glucose are unclear. Here, we describe the first comprehensive study of tryptophan aminotransferase and indole-3-pyruvate mono-oxygenase expression from 5 to 20 days after anthesis. A comparison of expression data with measurements of endogenous IAA via combined liquid chromatography–tandem mass spectrometry using heavy isotope labelled internal standards indicates that TaTAR2-B3, TaYUC9-A1, TaYUC9-B, TaYUC9-D1, TaYUC10-A and TaYUC10-D are primarily responsible for IAA production in developing grains. Furthermore, these genes are expressed specifically in developing grains, like those found in rice (Oryza sativa L.) and maize (Zea mays L.). Our results cast doubt on the proposed role of THOUSAND-GRAIN WEIGHT gene, TaTGW6, in promoting larger grain size via negative effects on grain IAA content. Work on this gene overlooked the contribution of IAA biosynthesis from tryptophan. Although IAA synthesis occurs primarily in the endosperm, we show the TaYUC9-1 group is also strongly expressed in the embryo. Within the endosperm, TaYUC9-1 expression is highest in aleurone and transfer cells, suggesting that IAA has a key role in differentiation of these tissues as has been proposed for other cereals.
Keywords: auxin, grain fill, TaTAR2, TaYUC, TaTGW6, TaTGW-7A, Triticum aestivum L., grain development, grain size.
References
Abu‐Zaitoon YM, Bennett K, Normanly J, Nonhebel HM (2012) A large increase in IAA during development of rice grains correlates with the expression of tryptophan aminotransferase OsTAR1 and a grain‐specific YUCCA. Physiologia Plantarum 146, 487–499.| A large increase in IAA during development of rice grains correlates with the expression of tryptophan aminotransferase OsTAR1 and a grain‐specific YUCCA.Crossref | GoogleScholarGoogle Scholar | 22582989PubMed |
Barkawi LS, Tam YY, Tillman JA, Pederson B, Calio J, Al-Amier H, Emerick M, Normanly J, Cohen JD (2008) A high-throughput method for the quantitative analysis of indole-3-acetic acid and other auxins from plant tissue. Analytical Biochemistry 372, 177–188.
| A high-throughput method for the quantitative analysis of indole-3-acetic acid and other auxins from plant tissue.Crossref | GoogleScholarGoogle Scholar | 17889819PubMed |
Basunia MA, Nonhebel HM (2019) Hormonal regulation of cereal endosperm development with a focus on rice (Oryza sativa). Functional Plant Biology 46, 493–506.
| Hormonal regulation of cereal endosperm development with a focus on rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar | 30955506PubMed |
Bernardi J, Lanubile A, Li Q-B, Kumar D, Kladnik A, Cook SD, Ross JJ, Marocco A, Chourey PS (2012) Impaired auxin biosynthesis in the defective endosperm18 mutant is due to mutational loss of expression in the ZmYuc1 gene encoding endosperm-specific YUCCA1 protein in maize. Plant Physiology 160, 1318–1328.
| Impaired auxin biosynthesis in the defective endosperm18 mutant is due to mutational loss of expression in the ZmYuc1 gene encoding endosperm-specific YUCCA1 protein in maize.Crossref | GoogleScholarGoogle Scholar | 22961134PubMed |
Bernardi J, Li QB, Gao Y, Zhao Y, Battaglia R, Marocco A, Chourey PS (2016) The auxin-deficient defective kernel18 (dek18) mutation alters the expression of seed-specific biosynthetic genes in maize. Journal of Plant Growth Regulation 35, 770–777.
| The auxin-deficient defective kernel18 (dek18) mutation alters the expression of seed-specific biosynthetic genes in maize.Crossref | GoogleScholarGoogle Scholar |
Bernardi J, Battaglia R, Bagnaresi P, Lucini L, Marocco A (2019) Transcriptomic and metabolomic analysis of ZmYUC1 mutant reveals the role of auxin during early endosperm formation in maize. Plant Science 281, 133–145.
| Transcriptomic and metabolomic analysis of ZmYUC1 mutant reveals the role of auxin during early endosperm formation in maize.Crossref | GoogleScholarGoogle Scholar | 30824046PubMed |
Borrill P, Ramirez-Gonzalez R, Uauy C (2016) expVIP: a customizable RNA-seq data analysis and visualization platform. Plant Physiology 170, 2172–2186.
| expVIP: a customizable RNA-seq data analysis and visualization platform.Crossref | GoogleScholarGoogle Scholar | 26869702PubMed |
Chen KH, Miller AN, Patterson GW, Cohen JD (1988) A rapid and simple procedure for purification of indole-3-acetic acid prior to GC-SIM-MS analysis. Plant Physiology 86, 822–825.
| A rapid and simple procedure for purification of indole-3-acetic acid prior to GC-SIM-MS analysis.Crossref | GoogleScholarGoogle Scholar | 16665995PubMed |
Choulet F, Alberti A, Theil S, Glover N, Barbe V, Daron J, Pingault L, Sourdille P, Couloux A, Paux E, et al (2014) Structural and functional partitioning of bread wheat chromosome 3B. Science 345, 1249721
| Structural and functional partitioning of bread wheat chromosome 3B.Crossref | GoogleScholarGoogle Scholar | 25035497PubMed |
Chourey PS, Li Q-B, Kumar D (2010) Sugar–hormone cross-talk in seed development: two redundant pathways of IAA biosynthesis are regulated differentially in the invertase-deficient miniature1 (mn1) seed mutant in maize. Molecular Plant 3, 1026–1036.
| Sugar–hormone cross-talk in seed development: two redundant pathways of IAA biosynthesis are regulated differentially in the invertase-deficient miniature1 (mn1) seed mutant in maize.Crossref | GoogleScholarGoogle Scholar | 20924026PubMed |
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 15034147PubMed |
FAOSTAT (2020) Food and Agriculture Organisation of the UN (FAO) statistics database: production, trade, supply. http://www.fao.org/faostat/en/#data/QC
Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783–791.
| Confidence limits on phylogenies: An approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar | 28561359PubMed |
Forestan C, Meda S, Varotto S (2010) ZmPIN1-mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm development. Plant Physiology 152, 1373–1390.
| ZmPIN1-mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm development.Crossref | GoogleScholarGoogle Scholar | 20044449PubMed |
Foulkes MJ, Slafer GA, Davies WJ, Berry PM, Sylvester-Bradley R, Martre P, Calderini DF, Griffiths S, Reynolds MP (2011) Raising yield potential of wheat. III. Optimizing partitioning to grain while maintaining lodging resistance. Journal of Experimental Botany 62, 469–486.
| Raising yield potential of wheat. III. Optimizing partitioning to grain while maintaining lodging resistance.Crossref | GoogleScholarGoogle Scholar | 20952627PubMed |
Guo T, Chen K, Dong NQ, Ye WW, Shan JX, Lin HX (2020) Tillering and small grain 1 dominates the tryptophan aminotransferase family required for local auxin biosynthesis in rice. Journal of Integrative Plant Biology 62, 581–600.
| Tillering and small grain 1 dominates the tryptophan aminotransferase family required for local auxin biosynthesis in rice.Crossref | GoogleScholarGoogle Scholar | 31081210PubMed |
Hu MJ, Zhang HP, Cao JJ, Zhu XF, Wang SX, Jiang H, Wu ZY, Lu J, Cheng C, Sun GL, Ma CX (2016a) Characterization of an IAA-glucose hydrolase gene TaTGW6 associated with grain weight in common wheat (Triticum aestivum L.). Molecular Breeding 36, 25
| Characterization of an IAA-glucose hydrolase gene TaTGW6 associated with grain weight in common wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |
Hu MJ, Zhang HP, Liu K, Cao JJ, Wang SX, Jiang H, Wu ZY, Lu J, Zhu XF, Xia XC, Sun GL, Ma CX, Chang C (2016b) Cloning and characterization of TaTGW-7A gene associated with grain weight in wheat via SLAF-seq-BSA. Frontiers in Plant Science 7, 1902
| Cloning and characterization of TaTGW-7A gene associated with grain weight in wheat via SLAF-seq-BSA.Crossref | GoogleScholarGoogle Scholar | 28066462PubMed |
Ishimaru K, Hirotsu N, Madoka Y, Murakami N, Hara N, Onodera H, Kashiwagi T, Ujiie K, Shimizu B, Onishi A, Miyagawa H, Katoh E (2013) Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nature Genetics 45, 707–711.
| Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield.Crossref | GoogleScholarGoogle Scholar | 23583977PubMed |
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8, 275–282.
| The rapid generation of mutation data matrices from protein sequences.Crossref | GoogleScholarGoogle Scholar |
Kersey PJ, Allen JE, Armean I, Boddu S, Bolt BJ, Carvalho-Silva D, Christensen M, Davis P, Falin LJ, Grabmueller C, et al (2016) Ensembl Genomes 2016: more genomes, more complexity. Nucleic Acids Research 44, D574–D580.
| Ensembl Genomes 2016: more genomes, more complexity.Crossref | GoogleScholarGoogle Scholar | 26578574PubMed |
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |
Li J, Chen S, Zhu L, Last RL (1995) Isolation of cDNAs encoding the tryptophan pathway enzyme indole-3-glycerol phosphate synthase from Arabidopsis thaliana. Plant Physiology 108, 877–878.
| Isolation of cDNAs encoding the tryptophan pathway enzyme indole-3-glycerol phosphate synthase from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 7610197PubMed |
Li N, Yin N, Niu Z, Hui W, Song J, Huang C, Wang H, Kong L, Feng D (2014) Isolation and characterization of three TaYUC10 genes from wheat. Gene 546, 187–194.
| Isolation and characterization of three TaYUC10 genes from wheat.Crossref | GoogleScholarGoogle Scholar | 24929126PubMed |
Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, McSteen P, Zhao Y, Hayashi KI, Kamiya Y, Kasahara H (2011) The main auxin biosynthesis pathway in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 108, 18512–18517.
| The main auxin biosynthesis pathway in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 22025724PubMed |
McAdam EL, Meitzel T, Quittenden LJ, Davidson SE, Dalmais M, Bendahmane AI, Thompson R, Smith JJ, Nichols DS, Urquhart S, Gelinas-Marion A, Aubert G, Ross JJ (2017) Evidence that auxin is required for normal seed size and starch synthesis in pea. New Phytologist 216, 193–204.
| Evidence that auxin is required for normal seed size and starch synthesis in pea.Crossref | GoogleScholarGoogle Scholar |
Meitzel T, Radchuk R, McAdam EL, Thormahlen I, Feil R, Munz E, Hilo A, Geigenberger P, Ross JJ, Lunn JE, Borisjuk L (2021) Trehalose 6-phosphate promotes seed filling by activating auxin biosynthesis. New Phytologist 229, 1553–1565.
| Trehalose 6-phosphate promotes seed filling by activating auxin biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Nolan T, Hands RE, Bustin SA (2006) Quantification of mRNA using real-time RT-PCR. Nature Protocols 1, 1559–1582.
| Quantification of mRNA using real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 17406449PubMed |
Nonhebel HM, Griffin K (2020) Production and roles of IAA and ABA during development of superior and inferior rice grains. Functional Plant Biology 47, 716–726.
| Production and roles of IAA and ABA during development of superior and inferior rice grains.Crossref | GoogleScholarGoogle Scholar | 32438973PubMed |
Paolacci AR, Tanzarella OA, Porceddu E, Ciaffi M (2009) Identification and validation of reference genes for quantitative RT-PCR normalization in wheat. BMC Molecular Biology 10, 11
| Identification and validation of reference genes for quantitative RT-PCR normalization in wheat.Crossref | GoogleScholarGoogle Scholar | 19232096PubMed |
Pfeifer M, Kugler KG, Sandve SR, Zhan B, Rudu H, Hvidsten TR, Mayer KFX, Olsen OA (2014) International Wheat Genome Sequencing Consortium. Genome interplay in the grain transcriptome of hexaploid bread wheat. Science 345, 1250091
| International Wheat Genome Sequencing Consortium. Genome interplay in the grain transcriptome of hexaploid bread wheat.Crossref | GoogleScholarGoogle Scholar | 25061194PubMed |
Ramírez-González RH, Borrill P, Land D, Harrington SA, Brinton J, Venturini L, Davey M, Jacobs J, Van Ex F, Pasha A, et al (2018) The transcriptional landscape of polyploid wheat. Science 361, eaar6089
| The transcriptional landscape of polyploid wheat.Crossref | GoogleScholarGoogle Scholar | 30115783PubMed |
Rhee SY, Beavis W, Berardini TZ, Chen G, Dixon D, Doyle A, Garcia-Hernandez M, Huala E, Lander G, Montoya M, Miller N, et al (2003) The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Research 31, 224–228.
| The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community.Crossref | GoogleScholarGoogle Scholar | 12519987PubMed |
Russell French S, Abu-Zaitoon Y, Uddin M, Bennett K, Nonhebel H (2014) Auxin and cell wall invertase related signaling during rice grain development. Plants 3, 95–112.
| Auxin and cell wall invertase related signaling during rice grain development.Crossref | GoogleScholarGoogle Scholar |
Shao A, Ma W, Zhao X, Hu M, He X, Teng W, Li H, Tong Y (2017) The auxin biosynthetic TRYPTOPHAN AMINOTRANSFERASE RELATED TaTAR2.1–3A increases wheat grain yield. Plant Physiology 174, 2274–2288.
| The auxin biosynthetic TRYPTOPHAN AMINOTRANSFERASE RELATED TaTAR2.1–3A increases wheat grain yield.Crossref | GoogleScholarGoogle Scholar | 28626005PubMed |
The International Wheat Genome Sequencing Consortium (IWGSC) (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361, eaar7191
| Shifting the limits in wheat research and breeding using a fully annotated reference genome.Crossref | GoogleScholarGoogle Scholar | 30262504PubMed |
Tuan PA, Yamasaki Y, Kanno Y, Seo M, Ayele BT (2019) Transcriptomics of cytokinin and auxin metabolism and signaling genes during seed maturation in dormant and non-dormant wheat genotypes. Scientific Reports 9, 3983
| Transcriptomics of cytokinin and auxin metabolism and signaling genes during seed maturation in dormant and non-dormant wheat genotypes.Crossref | GoogleScholarGoogle Scholar | 30850728PubMed |
Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y, Kasahara H, Kamiya Y, Chory J, Zhao Y (2011) Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 108, 18518–18523.
| Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 22025721PubMed |
Wu D, Dong J, Yao Y, Zhao W, Gao X (2015) Identification and evaluation of endogenous control genes for use in quantitative RT-PCR during wheat (Triticum aestivum L.) grain filling. Genetics and Molecular Research 14, 10530–10542.
| Identification and evaluation of endogenous control genes for use in quantitative RT-PCR during wheat (Triticum aestivum L.) grain filling.Crossref | GoogleScholarGoogle Scholar | 26400285PubMed |
Yamamoto Y, Kamiya N, Morinaka Y, Matsuoka M, Sazuka T (2007) Auxin biosynthesis by the YUCCA genes in rice. Plant Physiology 143, 1362–1371.
| Auxin biosynthesis by the YUCCA genes in rice.Crossref | GoogleScholarGoogle Scholar | 17220367PubMed |
Zhao D, MacKown CT, Starks PJ, Kindiger BK (2010) Rapid analysis of nonstructural carbohydrate components in grass forage using microplate enzymatic assays. Crop Science 50, 1537–1545.
| Rapid analysis of nonstructural carbohydrate components in grass forage using microplate enzymatic assays.Crossref | GoogleScholarGoogle Scholar |
Zhao Z, Zhang Y, Liu X, Zhang X, Liu S, Yu X, Ren Y, Zheng X, Zhou K, Jiang L, Guo X, Gai Y, Wu C, Zhai H, Wang H, Wan J (2013) A role for a dioxygenase in auxin metabolism and reproductive development in rice. Developmental Cell 27, 113–122.
| A role for a dioxygenase in auxin metabolism and reproductive development in rice.Crossref | GoogleScholarGoogle Scholar | 24094741PubMed |
Zou T, Li S, Liu M, Wang T, Xiao Q, Chen D, Li Q, Liang Y, Zhu J, Liang Y, Deng Q, Wang S, Zheng A, Wang L, Li P (2017) An atypical strictosidine synthase, OsSTRL2, plays key roles in anther development and pollen wall formation in rice. Scientific Reports 7, 6863
| An atypical strictosidine synthase, OsSTRL2, plays key roles in anther development and pollen wall formation in rice.Crossref | GoogleScholarGoogle Scholar | 28761138PubMed |
Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp. 97–166.