The Transcription Factor HaHB11 Boosts Grain Set and Yield in Rice Plants, Allowing Them to Approach Their Ideal Phenotype
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Material, Growth Conditions, and Treatments
2.2. Genetic Constructs
2.3. Rice Transformation
2.4. RNA Isolation and Expression Analyses with Real-Time RT-PCR
2.5. Crop Phenotyping
2.6. Green Index Evaluation
2.7. Histology
2.8. Brassinosteroid Treatment
2.9. Sequence Analyses
2.10. Statistical Analyses
2.11. Accession Numbers
3. Results
3.1. Rice Plants Constitutively Expressing HaHB11 Partition More Biomass to Leaves Than Controls and Exhibit Delayed Anthesis
3.2. In the Reproductive Stage, H11 Plants Exhibit Significantly Improved Traits Compared with Controls and pH11 Plants
3.3. The Uppermost Internode Length, Flag Leaf, and Tiller Angle in H11 Plants Contribute to Explaining Their Increased Yield
3.4. H11 Plants Exhibit Larger Vascular Bundles in Flag Leaf and Tiller Than Controls
3.5. H11 Flag Leaf Angles Are Insensitive to Brassinosteroids
3.6. The Constitutive Expression of the Sunflower HaHB11 Gene Is Necessary to Confer the Differential Traits
4. Discussion
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Izawa, T.; Shimamoto, K. Becoming a model plant: The importance of rice to plant science. Trends Plant Sci. 1996, 1, 95–99. [Google Scholar] [CrossRef]
- Peng, S.; Khush, G.S.; Virk, P.; Tang, Q.; Zou, Y. Progress in ideotype breeding to increase rice yield potential. Field Crops Res. 2008, 108, 32–38. [Google Scholar] [CrossRef]
- Yin, C.; Gan, L.; Ng, D.; Zhou, X.; Xia, K. Decreased panicle-derived indole-3-acetic acid reduces gibberellin A1 level in the uppermost internode, causing panicle enclosure in male sterile rice Zhenshan 97A. J. Exp. Bot. 2007, 58, 2441–2449. [Google Scholar] [PubMed]
- San, N.S.; Yamashita, M.; Adachi, S.; Tanabata, T.; Ookawa, T.; Hirasawa, T. Differences in lamina joint anatomy cause cultivar differences in leaf inclination angle of rice. Plant Prod. Sci. 2018, 21, 302–310. [Google Scholar] [CrossRef]
- Li, G.; Jain, R.; Chern, M.; Pham, N.T.; Martin, J.A.; Wei, T.; Schackwitz, W.S.; Lipzen, A.M.; Duong, P.Q.; Jones, K.C.; et al. The Sequences of 1504 Mutants in the Model Rice Variety Kitaake Facilitate Rapid Functional Genomic Studies. Plant Cell 2017, 29, 1218–1231. [Google Scholar] [PubMed]
- Li, L.; Shi, Z.Y.; Li, L.; Shen, G.Z.; Wang, X.Q.; An, L.S.; Zhang, J.L. Overexpression of ACL1 (abaxially curled leaf 1) increased Bulliform cells and induced Abaxial curling of leaf blades in rice. Mol. Plant 2010, 3, 807–817. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez, D.H. Introduction to transcription factor structure and function. In Plant Transcription Factors: Evolutionary, Structural and Functional Aspects; Elsevier: Amsterdam, The Netherlands, 2016; pp. 3–11. [Google Scholar]
- Hong, J.C. General Aspects of Plant Transcription Factor Families. In Plant Transcription Factors: Evolutionary, Structural and Functional Aspects; Elsevier: Amsterdam, The Netherlands, 2016; pp. 35–56. [Google Scholar]
- Perotti, M.F.; Ribone, P.A.; Chan, R.L. Plant transcription factors from the Homeodomain-Leucine Zipper family I. Role in development and stress responses. IUBMB Life 2017, 69, 280–289. [Google Scholar] [CrossRef]
- Arce, A.L.; Raineri, J.; Capella, M.; Cabello, J.V.; Chan, R.L. Uncharacterized conserved motifs outside the HD-Zip domain in HD-Zip subfamily I transcription factors; a potential source of functional diversity. BMC Plant Biol. 2011, 11, 42. [Google Scholar] [CrossRef]
- Capella, M.; Ré, D.A.; Arce, A.L.; Chan, R.L. Plant homeodomain-leucine zipper I transcription factors exhibit different functional AHA motifs that selectively interact with TBP or/and TFIIB. Plant Cell Rep. 2014, 33, 955967. [Google Scholar] [CrossRef]
- Spies, F.P.; Raineri, J.; Miguel, V.N.; Cho, Y.; Hong, J.C.; Chan, R.L. The Arabidopsis transcription factors AtPHL1 and AtHB23 act together promoting carbohydrate transport from pedicel-silique nodes to seeds. Plant Sci. 2022, 315, 111133. [Google Scholar] [CrossRef]
- Spies, F.P.; Perotti, M.F.; Cho, Y.; Jo, C.I.; Hong, J.C.; Chan, R.L. A complex tissue-specific interplay between the Arabidopsis transcription factors AtMYB68, AtHB23, and AtPHL1 modulates primary and lateral root development and adaptation to salinity. Plant J. 2023, in press. [Google Scholar] [CrossRef] [PubMed]
- Agalou, A.; Purwantomo, S.; Overnäs, E.; Johannesson, H.; Zhu, X.; Estiati, A.; de Kam, R.J.; Engström, P.; Slamet-Loedin, I.H.; Zhu, Z.; et al. A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members. Plant Mol. Biol. 2008, 66, 87–103. [Google Scholar] [CrossRef] [PubMed]
- Gao, S.; Fang, J.; Xu, F.; Wang, W.; Chu, C. Rice HOX12 Regulates Panicle Exsertion by Directly Modulating the Expression of ELONGATED UPPERMOST INTERNODE1. Plant Cell. 2016, 28, 680–695. [Google Scholar] [CrossRef] [PubMed]
- Hu, Y.; Li, S.; Fan, X.; Song, S.; Zhou, X.; Weng, X.; Xiao, J.; Li, X.; Xiong, L.; You, A.; et al. OsHOX1 and OsHOX28 Redundantly Shape Rice Tiller Angle by Reducing HSFA2D Expression and Auxin Content. Plant Physiol. 2020, 184, 1424–1437. [Google Scholar] [CrossRef] [PubMed]
- Bang, S.W.; Lee, D.K.; Jung, H.; Chung, P.J.; Kim, Y.S.; Choi, Y.D.; Suh, J.W.; Kim, J.K. Overexpression of OsTF1L, a rice HD-Zip transcription factor, promotes lignin biosynthesis and stomatal closure that improves drought tolerance. Plant Biotechnol. J. 2019, 17, 118–131. [Google Scholar] [CrossRef]
- Ribone, P.A.; Capella, M.; Arce, A.L.; Chan, R.L. What do we know about Homeodomain-Leucine Zipper I transcription factors? Functional and biotechnological considerations. In Plant Transcription Factors: Evolutionary, Structural and Functional Aspects; Daniel, G., Ed.; Academic Press: Cambridge, MA, USA; Elsevier: Amsterdam, The Netherlands, 2016; Chapter 22. [Google Scholar]
- Miguel, V.N.; Ribichich, K.F.; Giacomelli, J.I.; Chan, R.L. Key role of the motor protein Kinesin 13B in the activity of homeodomain-leucine zipper I transcription factors. J. Exp. Bot. 2020, 71, 6282–6296. [Google Scholar] [CrossRef]
- Cabello, J.V.; Giacomelli, J.I.; Piattoni, C.V.; Iglesias, A.A.; Chan, R.L. The sunflower transcription factor HaHB11 improves yield, biomass and tolerance to flooding in transgenic Arabidopsis plants. J. Biotechnol. 2016, 222, 73–83. [Google Scholar] [CrossRef]
- Cabello, J.V.; Giacomelli, J.I.; Gómez, M.C.; Chan, R.L. The sunflower transcription factor HaHB11 confers tolerance to water deficit and salinity to transgenic Arabidopsis and alfalfa plants. J. Biotechnol. 2017, 257, 35–46. [Google Scholar] [CrossRef]
- Raineri, J.; Campi, M.; Chan, R.L.; Otegui, M.E. Maize expressing the sunflower transcription factor HaHB11 has improved productivity in controlled and field conditions. Plant Sci. 2019, 287, 110185. [Google Scholar] [CrossRef]
- Raineri, J.; Caraballo, L.; Rigalli, N.; Portapila, M.; Otegui, M.E.; Chan, R.L. Expressing the sunflower transcription factor HaHB11 in maize improves waterlogging and defoliation tolerance. Plant Physiol. 2022, 189, 230–247. [Google Scholar] [CrossRef]
- Cabello, J.V.; Chan, R.L. Arabidopsis and sunflower plants with increased xylem area show enhanced seed yield. Plant J. 2019, 99, 717–732. [Google Scholar] [CrossRef]
- Estorninos, L.E., Jr.; Gealy, D.R.; Talbert, R.E.; Gbur, E.E. Rice and red rice interference. I. Response of red rice (Oryza sativa) to sowing rates of tropical japonica and indica rice cultivars. Weed Sci. 2005, 53, 676–682. [Google Scholar] [CrossRef]
- Main, M.; Frame, B.; Wang, K. Agrobacterium Protocols. In Methods in Molecular Biology 1223; Kan, W., Ed.; Springer: New York, NY, USA, 2015; Volume 1, Chapter 13. [Google Scholar]
- Gallo, K.P.; Daughtry, C.S.T. Techniques for measuring intercepted and absorbed photosynthetically active radiation in corn canopies. Agron. J. 2016, 78, 752–756. [Google Scholar] [CrossRef]
- Schneider, C.A.; Rasband, W.S.; Eliceiri, K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9, 671–675. [Google Scholar] [CrossRef] [PubMed]
- Li, H.Y.; Wang, H.M.; Jang, S. Rice Lamina Joint Inclination Assay. Bio-Protocol 2017, 7, e2409. [Google Scholar] [CrossRef] [PubMed]
- Needleman, S.B.; Wunsch, C.D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 1970, 48, 443–453. [Google Scholar] [CrossRef]
- Peng, S.; Cassman, K.G.; Virmani, S.S.; Sheehy, J.E.; Khush, G.S. Yield potential trends of tropical rice since the release of IR8 and the challenge of increasing rice yield potential. Crop Sci. 1999, 39, 1552–1559. [Google Scholar] [CrossRef]
- Dingkuhn, M.; Laza, M.R.C.; Kumar, U.; Mendez, K.S.; Collard, B.; Jagadish, K.; Singh, R.K.; Padolina, T.; Malabayabas, M.; Torres, E.; et al. Improving yield potential of tropical rice: Achieved levels and perspectives through improved ideotypes. Field Crops Res. 2015, 182, 43–59. [Google Scholar] [CrossRef]
- Luo, A.; Qian, Q.; Yin, H.; Liu, X.; Yin, C.; Lan, Y.; Tang, J.; Tang, Z.; Cao, S.; Wang, X.; et al. EUI1, encoding a putative cytochrome P450 monooxygenase, regulates internode elongation by modulating gibberellin responses in rice. Plant Cell Physiol. 2006, 47, 181–191. [Google Scholar] [CrossRef]
- Zhu, Y.; Nomura, T.; Xu, Y.; Zhang, Y.; Peng, Y.; Mao, B.; Hanada, A.; Zhou, H.; Wang, R.; Li, P.; et al. ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 2006, 18, 442–456. [Google Scholar] [CrossRef]
- Zhang, B.; Ye, W.; Ren, D.; Tian, P.; Peng, Y.; Gao, Y.; Ruan, B.; Wang, L.; Zhang, G.; Guo, L.; et al. Genetic analysis of flag leaf size and candidate genes determination of a major QTL for flag leaf width in rice. Rice 2015, 8, 39. [Google Scholar] [CrossRef]
- Zou, L.P.; Sun, X.H.; Zhang, Z.G.; Liu, P.; Wu, J.X.; Tian, C.J.; Qiu, J.L.; Lu, T.G. Leaf rolling controlled by the homeodomain leucine zipper class IV gene Roc5 in rice. Plant Physiol. 2011, 156, 1589–1602. [Google Scholar] [CrossRef]
- Wang, J.J.; Xu, J.; Qian, Q.; Zhang, G.H. Development of rice leaves: How histiocytic cells modulate leaf polarity establishment. Rice Sci. 2020, 27, 468–479. [Google Scholar]
- Komatsuda, T.; Pourkheirandish, M.; He, C.; Azhaguvel, P.; Kanamori, H.; Perovic, D.; Stein, N.; Graner, A.; Wicker, T.; Tagiri, A.; et al. Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc. Natl. Acad. Sci. USA 2007, 104, 1424–1429. [Google Scholar] [CrossRef] [PubMed]
- Ren, X.; Wang, Y.; Yan, S.; Sun, D.; Sun, G. Population genetics and phylogenetic analysis of the vrs1 nucleotide sequence in wild and cultivated barley. Genome 2014, 57, 239–244. [Google Scholar] [CrossRef]
- Shao, J.; Haider, I.; Xiong, L.; Zhu, X.; Hussain, R.M.F.; Övernäs, E.; Meijer, A.H.; Zhang, G.; Wang, M.; Bouwmeester, H.J.; et al. Functional analysis of the HD-Zip transcription factor genes Oshox12 and Oshox14 in rice. PLoS ONE 2018, 13, e0199248. [Google Scholar] [CrossRef]
- González, F.G.; Capella, M.; Ribichich, K.F.; Curín, F.; Giacomelli, J.I.; Ayala, F.; Watson, G.; Otegui, M.E.; Chan, R.L. Field-grown transgenic wheat expressing the sunflower gene HaHB4 significantly outyields the wild type. J. Exp. Bot. 2019, 70, 1669–1681. [Google Scholar] [CrossRef] [PubMed]
- Xiong, M.; Feng, G.; Gao, Q.; Zhang, C.; Li, Q.; Liu, Q.Q. Brassinosteroid regulation in rice seed biology. Seed Biol. 2022, 1, 1–9. [Google Scholar] [CrossRef]
- Li, Q.F.; Lu, J.; Zhou, Y.; Wu, F.; Tong, H.N.; Wang, J.D.; Yu, J.W.; Zhang, C.Q.; Fan, X.L.; Liu, Q.Q. Abscisic Acid Represses Rice Lamina Joint Inclination by Antagonizing Brassinosteroid Biosynthesis and Signaling. Int. J. Mol. Sci. 2019, 20, 4908. [Google Scholar] [CrossRef]
- Sakamoto, T.; Morinaka, Y.; Ohnishi, T.; Sunohara, H.; Fujioka, S.; Ueguchi-Tanaka, M.; Mizutani, M.; Sakata, K.; Takatsuto, S.; Yoshida, S.; et al. Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat. Biotechnol. 2006, 24, 105–109. [Google Scholar] [CrossRef]
- Kumar, S.; Tripathi, S.; Singh, S.P.; Prasad, A.; Akter, F.; Syed, M.A.; Badri, J.; Das, S.P.; Bhattarai, R.; Natividad, M.A.; et al. Rice breeding for yield under drought has selected for longer flag leaves and lower stomatal density. J. Exp. Bot. 2021, 72, 4981–4992. [Google Scholar] [CrossRef] [PubMed]
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Raineri, J.; Caraballo, L.N.; Gómez, M.; Chan, R.L. The Transcription Factor HaHB11 Boosts Grain Set and Yield in Rice Plants, Allowing Them to Approach Their Ideal Phenotype. Biomolecules 2023, 13, 826. https://doi.org/10.3390/biom13050826
Raineri J, Caraballo LN, Gómez M, Chan RL. The Transcription Factor HaHB11 Boosts Grain Set and Yield in Rice Plants, Allowing Them to Approach Their Ideal Phenotype. Biomolecules. 2023; 13(5):826. https://doi.org/10.3390/biom13050826
Chicago/Turabian StyleRaineri, Jesica, Luciano Nicolás Caraballo, Maximiliano Gómez, and Raquel Lía Chan. 2023. "The Transcription Factor HaHB11 Boosts Grain Set and Yield in Rice Plants, Allowing Them to Approach Their Ideal Phenotype" Biomolecules 13, no. 5: 826. https://doi.org/10.3390/biom13050826