Improved reproductive growth of euhalophyte Suaeda salsa under salinity is correlated with altered phytohormone biosynthesis and signal transduction
Jianrong Guo A , Chaoxia Lu A , Fangcheng Zhao A , Shuai Gao A and Baoshan Wang
A B
+ Author Affiliations
- Author Affiliations
A Shandong Provincial Key Laboratory of Plant Stress, College of Life Science, Shandong Normal University, Ji’nan, Shandong, 250014, PR China.
B Corresponding author. Email: bswang@sdnu.edu.cn
Functional Plant Biology 47(2) 170-183 https://doi.org/10.1071/FP19215
Submitted: 4 August 2019 Accepted: 20 October 2019 Published: 16 January 2020
Abstract
Phytohormones are essential for plant reproductive growth. Salinity limits crop reproductive growth and yield, but improves reproductive growth of euhalophytes. However, little is known about the mechanisms underlying salinity’s effects on plant reproductive growth. To elucidate the role of plant hormones in flower development of the euhalophyte Suaeda salsa under saline conditions, we analysed endogenous gibberellic acid (GA3,4), indoleacetic acid (IAA), zeatin riboside (ZR), abscisic acid (ABA), and brassinosteroids (BRs) during flowering in control (0 mM) and NaCl-treated (200 mM) plants. At the end of vegetative growth, endogenous GA3, GA4, ABA and BR contents in stems of NaCl-treated plants were significantly higher than those in controls. During flowering, GA3, GA4, IAA and ZR contents showed the most significant enhancement in flower organs of plants treated with NaCl when compared with controls. Additionally, genes related to ZR, IAA, GA, BR and ABA biosynthesis and plant hormone signal transduction, such as those encoding CYP735A, CYP85A, GID1, NCED, PIF4, AHP, TCH4, SnRK2 and ABF, were upregulated in S. salsa flowers from NaCl-treated plants. These results suggest that coordinated upregulation of genes involved in phytohormone biosynthesis and signal transduction contributes to the enhanced reproductive growth of S. salsa under salinity.
Additional keywords: flower development, NaCl, plant hormones, Suaeda salsa, transcriptome.
References
Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M (2004) UniProt: the universal protein knowledgebase. Nucleic Acids Research 32, 115D–119D.| UniProt: the universal protein knowledgebase.Crossref | GoogleScholarGoogle Scholar |
Arrom L, Munné-Bosch S (2012) Hormonal changes during flower development in floral tissues of Lilium. Planta 236, 343–354.
| Hormonal changes during flower development in floral tissues of Lilium.Crossref | GoogleScholarGoogle Scholar | 22367063PubMed |
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT (2000) Gene ontology: tool for the unification of biology. Nature Genetics 25, 25–29.
| Gene ontology: tool for the unification of biology.Crossref | GoogleScholarGoogle Scholar | 10802651PubMed |
Azoulay-Shemer T, Palomares A, Bagheri A, Israelsson‐Nordstrom M, Engineer CB, Bargmann BO, Stephan AB, Schroeder JI (2015) Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO2-and ABA-induced stomatal closing. The Plant Journal 83, 567–581.
Barazesh S, McSteen P (2008) Hormonal control of grass inflorescence development. Trends in Plant Science 13, 656–662.
| Hormonal control of grass inflorescence development.Crossref | GoogleScholarGoogle Scholar | 18986827PubMed |
Bartrina I, Otto E, Strnad M, Werner T, Schmülling T (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. The Plant Cell 23, 69–80.
| Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 21224426PubMed |
Brumos J, Robles LM, Yun J, Vu TC, Jackson S, Alonso JM, Stepanova AN (2018) Local auxin biosynthesis is a key regulator of plant development. Developmental Cell 47, 306–318.e5.
| Local auxin biosynthesis is a key regulator of plant development.Crossref | GoogleScholarGoogle Scholar | 30415657PubMed |
Campos KO, Kerbauy GB (2004) Thermoperiodic effect on flowering and endogenous hormonal status in Dendrobium (Orchidaceae). Journal of Plant Physiology 161, 1385–1387.
| Thermoperiodic effect on flowering and endogenous hormonal status in Dendrobium (Orchidaceae).Crossref | GoogleScholarGoogle Scholar | 15658809PubMed |
Cecchetti V, Celebrin D, Napoli N, Ghelli R, Brunetti P, Costantino P, Cardarelli M (2017) An auxin maximum in the middle layer controls stamen development and pollen maturation in Arabidopsis. New Phytologist 213, 1194–1207.
| An auxin maximum in the middle layer controls stamen development and pollen maturation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 27659765PubMed |
Chandler JW (2011) Founder cell specification. Trends in Plant Science 16, 607–613.
| Founder cell specification.Crossref | GoogleScholarGoogle Scholar | 21924666PubMed |
Chang MZ, Huang CH (2018) Effects of GA3 on promotion of flowering in Kalanchoe spp. Scientia Horticulturae 238, 7–13.
| Effects of GA3 on promotion of flowering in Kalanchoe spp.Crossref | GoogleScholarGoogle Scholar |
Cheng ZJ, Zhao XY, Shao XX, Wang F, Zhou C, Liu YG, Zhang Y, Zhang XS (2014) Abscisic acid regulates early seed development in Arabidopsis by ABI5-mediated transcription of SHORT HYPOCOTYL UNDER BLUE1. The Plant Cell 26, 1053–1068.
| Abscisic acid regulates early seed development in Arabidopsis by ABI5-mediated transcription of SHORT HYPOCOTYL UNDER BLUE1.Crossref | GoogleScholarGoogle Scholar | 24619610PubMed |
Corbesier L, Prinsen E, Jacqmard A, Lejeune P, Van Onckelen H, Périlleux C, Bernier G (2003) Cytokinin levels in leaves, leaf exudate and shoot apical meristem of Arabidopsis thaliana during floral transition. Journal of Experimental Botany 54, 2511–2517.
| Cytokinin levels in leaves, leaf exudate and shoot apical meristem of Arabidopsis thaliana during floral transition.Crossref | GoogleScholarGoogle Scholar | 14512385PubMed |
Cucinotta M, Manrique S, Guazzotti A, Quadrelli NE, Mendes MA, Benkova E, Colombo L (2016) Cytokinin response factors integrate auxin and cytokinin pathways for female reproductive organ development. Development 143, 4419–4424.
| Cytokinin response factors integrate auxin and cytokinin pathways for female reproductive organ development.Crossref | GoogleScholarGoogle Scholar | 27737904PubMed |
Cui Z, Zhou B, Zhang Z, Hu Z (2013) Abscisic acid promotes flowering and enhances LcAP1 expression in Litchi chinensis Sonn. South African Journal of Botany 88, 76–79.
| Abscisic acid promotes flowering and enhances LcAP1 expression in Litchi chinensis Sonn.Crossref | GoogleScholarGoogle Scholar |
Davidson NM, Oshlack A (2014) Corset: enabling differential gene expression analysis for de novo assembled transcriptomes. Genome Biology 15, 410
Eriksson S, Böhlenius H, Moritz T, Nilsson O (2006) GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation. The Plant Cell 18, 2172–2181.
| GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation.Crossref | GoogleScholarGoogle Scholar | 16920780PubMed |
Fang L, Su L, Sun X, Li X, Sun M, Karungo SK, Fang S, Chu J, Li S, Xin H (2016) Expression of Vitis amurensis NAC26 in Arabidopsis enhances drought tolerance by modulating jasmonic acid synthesis. Journal of Experimental Botany 67, 2829–2845.
| Expression of Vitis amurensis NAC26 in Arabidopsis enhances drought tolerance by modulating jasmonic acid synthesis.Crossref | GoogleScholarGoogle Scholar | 27162276PubMed |
Fariduddin Q, Yusuf M, Ahmad I, Ahmad A (2014) Brassinosteroids and their role in response of plants to abiotic stresses. Biologia Plantarum 58, 9–17.
| Brassinosteroids and their role in response of plants to abiotic stresses.Crossref | GoogleScholarGoogle Scholar |
Ferreira LG, de Alencar Dusi DM, Irsigler AST, Gomes ACMM, Mendes MA, Colombo L, de Campos Carneiro VT (2018) GID1 expression is associated with ovule development of sexual and apomictic plants. Plant Cell Reports 37, 293–306.
| GID1 expression is associated with ovule development of sexual and apomictic plants.Crossref | GoogleScholarGoogle Scholar | 29080908PubMed |
Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. The Plant Cell 14, S15–S45.
Fu J, Chu J, Sun X, Wang J, Yan C (2012) Simple, rapid, and simultaneous assay of multiple carboxyl containing phytohormones in wounded tomatoes by UPLC-MS/MS using single SPE purification and isotope dilution. Analytical Sciences 28, 1081–1087.
| Simple, rapid, and simultaneous assay of multiple carboxyl containing phytohormones in wounded tomatoes by UPLC-MS/MS using single SPE purification and isotope dilution.Crossref | GoogleScholarGoogle Scholar | 23149609PubMed |
Gallavotti A, Barazesh S, Malcomber S, Hall D, Jackson D, Schmidt RJ, McSteen P (2008) sparse inflorescence1 encodes a monocot-specific YUCCA-like gene required for vegetative and reproductive development in maize. Proceedings of the National Academy of Sciences of the United States of America 105, 15196–15201.
| sparse inflorescence1 encodes a monocot-specific YUCCA-like gene required for vegetative and reproductive development in maize.Crossref | GoogleScholarGoogle Scholar | 18799737PubMed |
Ghelli R, Brunetti P, Napoli N, De Paolis A, Cecchetti V, Tsuge T, Serino G, Matsui M, Mele G, Rinaldi G (2018) A newly identified flower-specific splice variant of AUXIN RESPONSE FACTOR8 regulates stamen elongation and endothecium lignification in Arabidopsis. The Plant Cell 30, 620–637.
| A newly identified flower-specific splice variant of AUXIN RESPONSE FACTOR8 regulates stamen elongation and endothecium lignification in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 29514943PubMed |
Gómez-Cadenas A, Zentella R, Walker-Simmons MK, Ho T-HD (2001) Gibberellin/abscisic acid antagonism in barley aleurone cells: site of action of the protein kinase PKABA1 in relation to gibberellin signaling molecules. The Plant Cell 13, 667–679.
| Gibberellin/abscisic acid antagonism in barley aleurone cells: site of action of the protein kinase PKABA1 in relation to gibberellin signaling molecules.Crossref | GoogleScholarGoogle Scholar | 11251104PubMed |
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nature Biotechnology 29, 644
| Full-length transcriptome assembly from RNA-seq data without a reference genome.Crossref | GoogleScholarGoogle Scholar | 21572440PubMed |
Guo J, Suo S, Wang B-S (2015) Sodium chloride improves seed vigour of the euhalophyte Suaeda salsa. Seed Science Research 25, 335–344.
| Sodium chloride improves seed vigour of the euhalophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar |
Guo J, Li Y, Han G, Song J, Wang B (2018) NaCl markedly improved the reproductive capacity of the euhalophyte Suaeda salsa. Functional Plant Biology 45, 350–361.
| NaCl markedly improved the reproductive capacity of the euhalophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar |
Guo J, Dong X, Han G, Wang B (2019) Salt-enhanced reproductive development of Suaeda salsa L. coincided with ion transporter gene upregulation in flowers and increased pollen K+ content. Frontiers of Plant Science 10, 333
| Salt-enhanced reproductive development of Suaeda salsa L. coincided with ion transporter gene upregulation in flowers and increased pollen K+ content.Crossref | GoogleScholarGoogle Scholar |
Han G, Yuan F, Guo J, Zhang Y, Sui N, Wang B (2019) AtSIZ1 improves salt tolerance by maintaining ionic homeostasis and osmotic balance in Arabidopsis. Plant Science 285, 55–67.
| AtSIZ1 improves salt tolerance by maintaining ionic homeostasis and osmotic balance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 31203894PubMed |
Hu J, Mitchum MG, Barnaby N, Ayele BT, Ogawa M, Nam E, Lai W-C, Hanada A, Alonso JM, Ecker JR (2008) Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. The Plant Cell 20, 320–336.
| Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 18310462PubMed |
Kakimoto T (2003) Perception and signal transduction of cytokinins. Annual Review of Plant Biology 54, 605–627.
| Perception and signal transduction of cytokinins.Crossref | GoogleScholarGoogle Scholar | 14503005PubMed |
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T (2007) KEGG for linking genomes to life and the environment. Nucleic Acids Research 36, D480–D484.
| KEGG for linking genomes to life and the environment.Crossref | GoogleScholarGoogle Scholar | 18077471PubMed |
Khatun S, Flowers T (1995) The estimation of pollen viability in rice. Journal of Experimental Botany 46, 151–154.
| The estimation of pollen viability in rice.Crossref | GoogleScholarGoogle Scholar |
Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T (2005) Abscisic acid‐activated SNRK2 protein kinases function in the gene‐regulation pathway of ABA signal transduction by phosphorylating ABA response element‐binding factors. The Plant Journal 44, 939–949.
| Abscisic acid‐activated SNRK2 protein kinases function in the gene‐regulation pathway of ABA signal transduction by phosphorylating ABA response element‐binding factors.Crossref | GoogleScholarGoogle Scholar | 16359387PubMed |
Krizek BA (2011) Auxin regulation of Arabidopsis flower development involves members of the AINTEGUMENTA-LIKE/PLETHORA (AIL/PLT) family. Journal of Experimental Botany 62, 3311–3319.
| Auxin regulation of Arabidopsis flower development involves members of the AINTEGUMENTA-LIKE/PLETHORA (AIL/PLT) family.Crossref | GoogleScholarGoogle Scholar | 21511900PubMed |
Larsson E, Vivian-Smith A, Offringa R, Sundberg E (2017) Auxin homeostasis in Arabidopsis ovules is anther-dependent at maturation and changes dynamically upon fertilization. Frontiers of Plant Science 8, 1735
| Auxin homeostasis in Arabidopsis ovules is anther-dependent at maturation and changes dynamically upon fertilization.Crossref | GoogleScholarGoogle Scholar |
Le B, Nawaz MA, Rehman HM, Le T, Yang SH, Golokhvast KS, Son E, Chung G (2016) Genome-wide characterization and expression pattern of auxin response factor (ARF) gene family in soybean and common bean. Genes & Genomics 38, 1165–1178.
| Genome-wide characterization and expression pattern of auxin response factor (ARF) gene family in soybean and common bean.Crossref | GoogleScholarGoogle Scholar |
Li W, Liu X, Khan MA, Yamaguchi S (2005) The effect of plant growth regulators, nitric oxide, nitrate, nitrite and light on the germination of dimorphic seeds of Suaeda salsa under saline conditions. Journal of Plant Research 118, 207–214.
| The effect of plant growth regulators, nitric oxide, nitrate, nitrite and light on the germination of dimorphic seeds of Suaeda salsa under saline conditions.Crossref | GoogleScholarGoogle Scholar | 15937723PubMed |
Li X, Zhang X, Song J, Fan H, Feng G, Wang B (2011) Accumulation of ions during seed development under controlled saline conditions of two Suaeda salsa populations is related to their adaptation to saline environments. Plant and Soil 341, 99–107.
| Accumulation of ions during seed development under controlled saline conditions of two Suaeda salsa populations is related to their adaptation to saline environments.Crossref | GoogleScholarGoogle Scholar |
Liu J, Chu J, Ma C, Jiang Y, Ma Y, Xiong J, Cheng Z-M (2019) Overexpression of an ABA-dependent grapevine bZIP transcription factor, VvABF2, enhances osmotic stress in Arabidopsis. Plant Cell Reports 38, 587–596.
| Overexpression of an ABA-dependent grapevine bZIP transcription factor, VvABF2, enhances osmotic stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 30712103PubMed |
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15, 550
| Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.Crossref | GoogleScholarGoogle Scholar | 25516281PubMed |
Lu C, Qiu N, Wang B, Zhang J (2003) Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. Journal of Experimental Botany 54, 851–860.
| Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar | 12554728PubMed |
Lv B, Yan Z, Tian H, Zhang X, Ding Z (2019) Local auxin biosynthesis mediates plant growth and development. Trends in Plant Science 24, 6–9.
| Local auxin biosynthesis mediates plant growth and development.Crossref | GoogleScholarGoogle Scholar | 30448230PubMed |
Ma Q, Zhou X, Wu G, Wang S (2009a) Cloning and sequence analysis of actin gene fragment from the halophyte Suaeda glauca. Biotechnology 19, 1–3.
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009b) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324, 1064–1068.
Mahouachi J, Gómez-Cadenas A, Primo-Millo E, Talon M (2005) Antagonistic changes between abscisic acid and gibberellins in citrus fruits subjected to a series of different water conditions. Journal of Plant Growth Regulation 24, 179–187.
| Antagonistic changes between abscisic acid and gibberellins in citrus fruits subjected to a series of different water conditions.Crossref | GoogleScholarGoogle Scholar |
Mignolli F, Vidoz ML, Picciarelli P, Mariotti L (2018) Gibberellins modulate auxin responses during tomato (Solanum lycopersicum L.) fruit development. Physiologia Plantarum 165, 768–779.
| Gibberellins modulate auxin responses during tomato (Solanum lycopersicum L.) fruit development.Crossref | GoogleScholarGoogle Scholar | 29888535PubMed |
Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132, 4107–4118.
| Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation.Crossref | GoogleScholarGoogle Scholar | 16107481PubMed |
Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2. 2, SRK2E/SnRK2. 6/OST1 and SRK2I/SnRK2. 3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant & Cell Physiology 50, 1345–1363.
| Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2. 2, SRK2E/SnRK2. 6/OST1 and SRK2I/SnRK2. 3, involved in ABA signaling are essential for the control of seed development and dormancy.Crossref | GoogleScholarGoogle Scholar |
Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. The Plant Cell 23, 2169–2183.
| Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis.Crossref | GoogleScholarGoogle Scholar | 21719693PubMed |
Onyemaobi I, Liu H, Siddique KH, Yan G (2017) Both male and female malfunction contributes to yield reduction under water stress during meiosis in bread wheat. Frontiers of Plant Science 7, 2071
| Both male and female malfunction contributes to yield reduction under water stress during meiosis in bread wheat.Crossref | GoogleScholarGoogle Scholar |
Pakkish Z, Hossien Poor M, Akbar Nasab M, Asghari H (2019) Brassinolides have a small effect on vegetative growth, and increase reproductive growth of pistachio trees cv. Owhadi. Journal of Horticultural Science & Biotechnology 94, 118–122.
| Brassinolides have a small effect on vegetative growth, and increase reproductive growth of pistachio trees cv. Owhadi.Crossref | GoogleScholarGoogle Scholar |
Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Tsz-fung FC (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068–1071.
Peres ALG, Soares JS, Tavares RG, Righetto G, Zullo MA, Mandava NB, Menossi M (2019) Brassinosteroids, the sixth class of phytohormones: a molecular view from the discovery to hormonal interactions in plant development and stress adaptation. International Journal of Molecular Sciences 20, 331
| Brassinosteroids, the sixth class of phytohormones: a molecular view from the discovery to hormonal interactions in plant development and stress adaptation.Crossref | GoogleScholarGoogle Scholar |
Plackett AR, Thomas SG, Wilson ZA, Hedden P (2011) Gibberellin control of stamen development: a fertile field. Trends in Plant Science 16, 568–578.
| Gibberellin control of stamen development: a fertile field.Crossref | GoogleScholarGoogle Scholar | 21824801PubMed |
Premkumar G, Sankaranarayanan R, Jeeva S, Rajarathinam K (2011) Cytokinin induced shoot regeneration and flowering of Scoparia dulcis L. (Scrophulariaceae) – an ethnomedicinal herb. Asian Pacific Journal of Tropical Biomedicine 1, 169–172.
| Cytokinin induced shoot regeneration and flowering of Scoparia dulcis L. (Scrophulariaceae) – an ethnomedicinal herb.Crossref | GoogleScholarGoogle Scholar | 23569752PubMed |
Pruitt KD, Tatusova T, Maglott DR (2005) NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Research 33, D501–D504.
| NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins.Crossref | GoogleScholarGoogle Scholar | 15608248PubMed |
Przemeck GK, Mattsson J, Hardtke CS, Sung ZR, Berleth T (1996) Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta 200, 229–237.
| Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization.Crossref | GoogleScholarGoogle Scholar | 8904808PubMed |
Ryu H, Cho Y-G (2015) Plant hormones in salt stress tolerance. Journal of Plant Biology 58, 147–155.
| Plant hormones in salt stress tolerance.Crossref | GoogleScholarGoogle Scholar |
Sakurai A, Fujioka S (1993) The current status of physiology and biochemistry of brassinosteroids. Plant Growth Regulation 13, 147–159.
| The current status of physiology and biochemistry of brassinosteroids.Crossref | GoogleScholarGoogle Scholar |
Santiago J, Dupeux F, Round A, Antoni R, Park S-Y, Jamin M, Cutler SR, Rodriguez PL, Márquez JA (2009) The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462, 665–668.
| The abscisic acid receptor PYR1 in complex with abscisic acid.Crossref | GoogleScholarGoogle Scholar | 19898494PubMed |
Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133, 251–261.
| The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs.Crossref | GoogleScholarGoogle Scholar | 16339187PubMed |
Sessions A, Nemhauser JL, McColl A, Roe JL, Feldmann KA, Zambryski PC (1997) ETTIN patterns the Arabidopsis floral meristem and reproductive organs. Development 124, 4481–4491.
Shu K, Zhou W, Chen F, Luo X, Yang W (2018) Abscisic acid and gibberellins antagonistically mediate plant development and abiotic stress responses. Frontiers of Plant Science 9, 416
| Abscisic acid and gibberellins antagonistically mediate plant development and abiotic stress responses.Crossref | GoogleScholarGoogle Scholar |
Siddiqui H, Hayat S, Bajguz A (2018) Regulation of photosynthesis by brassinosteroids in plants. Acta Physiologiae Plantarum 40, 59
| Regulation of photosynthesis by brassinosteroids in plants.Crossref | GoogleScholarGoogle Scholar |
Song J, Wang B (2015) Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Annals of Botany 115, 541–553.
| Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model.Crossref | GoogleScholarGoogle Scholar | 25288631PubMed |
Song J, Fan H, Zhao Y, Jia Y, Du X, Wang B (2008) Effect of salinity on germination, seedling emergence, seedling growth and ion accumulation of a euhalophyte Suaeda salsa in an intertidal zone and on saline inland. Aquatic Botany 88, 331–337.
| Effect of salinity on germination, seedling emergence, seedling growth and ion accumulation of a euhalophyte Suaeda salsa in an intertidal zone and on saline inland.Crossref | GoogleScholarGoogle Scholar |
Song J, Chen M, Feng G, Jia Y, Wang B, Zhang F (2009) Effect of salinity on growth, ion accumulation and the roles of ions in osmotic adjustment of two populations of Suaeda salsa. Plant and Soil 314, 133–141.
| Effect of salinity on growth, ion accumulation and the roles of ions in osmotic adjustment of two populations of Suaeda salsa.Crossref | GoogleScholarGoogle Scholar |
Song J, Shi G, Gao B, Fan H, Wang B (2011) Waterlogging and salinity effects on two Suaeda salsa populations. Physiologia Plantarum 141, 343–351.
| Waterlogging and salinity effects on two Suaeda salsa populations.Crossref | GoogleScholarGoogle Scholar | 21214881PubMed |
Song J, Zhou J, Zhao W, Xu H, Wang F, Xu Y, Wang L, Tian C (2016) Effects of salinity and nitrate on production and germination of dimorphic seeds applied both through the mother plant and exogenously during germination in Suaeda salsa. Plant Species Biology 31, 19–28.
| Effects of salinity and nitrate on production and germination of dimorphic seeds applied both through the mother plant and exogenously during germination in Suaeda salsa.Crossref | GoogleScholarGoogle Scholar |
Sreenivasulu N, Harshavardhan VT, Govind G, Seiler C, Kohli A (2012) Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene 506, 265–273.
| Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress?Crossref | GoogleScholarGoogle Scholar | 22771691PubMed |
Suge H (1986) Reproductive development of higher plants as influenced by brassinolide. Plant & Cell Physiology 27, 199–205.
Sui N, Yang Z, Liu M, Wang B (2015) Identification and transcriptomic profiling of genes involved in increasing sugar content during salt stress in sweet sorghum leaves. BMC Genomics 16, 534
| Identification and transcriptomic profiling of genes involved in increasing sugar content during salt stress in sweet sorghum leaves.Crossref | GoogleScholarGoogle Scholar | 26186930PubMed |
Swain SM, Singh DP (2005) Tall tales from sly dwarves: novel functions of gibberellins in plant development. Trends in Plant Science 10, 123–129.
| Tall tales from sly dwarves: novel functions of gibberellins in plant development.Crossref | GoogleScholarGoogle Scholar | 15749470PubMed |
Tang Y, Bao X, Liu K, Wang J, Zhang J, Feng Y, Wang Y, Lin L, Feng J, Li C (2018) Genome-wide identification and expression profiling of the auxin response factor (ARF) gene family in physic nut. PLoS One 13, e0201024
| Genome-wide identification and expression profiling of the auxin response factor (ARF) gene family in physic nut.Crossref | GoogleScholarGoogle Scholar | 30592727PubMed |
Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Research 28, 33–36.
| The COG database: a tool for genome-scale analysis of protein functions and evolution.Crossref | GoogleScholarGoogle Scholar | 10592175PubMed |
Tiwari VK, Stadler MB, Wirbelauer C, Paro R, Schübeler D, Beisel C (2012) A chromatin-modifying function of JNK during stem cell differentiation. Nature Genetics 44, 94–100.
| A chromatin-modifying function of JNK during stem cell differentiation.Crossref | GoogleScholarGoogle Scholar |
Vardhini BV, Anjum NA (2015) Brassinosteroids make plant life easier under abiotic stresses mainly by modulating major components of antioxidant defense system. Frontiers in Environmental Science 2, 67
| Brassinosteroids make plant life easier under abiotic stresses mainly by modulating major components of antioxidant defense system.Crossref | GoogleScholarGoogle Scholar |
Viger M, Hancock RD, Miglietta F, Taylor G (2015) More plant growth but less plant defence? First global gene expression data for plants grown in soil amended with biochar. Global Change Biology. Bioenergy 7, 658–672.
| More plant growth but less plant defence? First global gene expression data for plants grown in soil amended with biochar.Crossref | GoogleScholarGoogle Scholar |
Wang YH, Irving HR (2011) Developing a model of plant hormone interactions. Plant Signaling & Behavior 6, 494–500.
| Developing a model of plant hormone interactions.Crossref | GoogleScholarGoogle Scholar |
Wang F, Yin C, Song Y, Li Q, Tian C, Song J (2018) Reproductive allocation and fruit-set pattern in the euhalophyte Suaeda salsa in controlled and field conditions. Plant Biosystems-An International Journal Dealing with all Aspects of Plant Biology 152, 749–758.
| Reproductive allocation and fruit-set pattern in the euhalophyte Suaeda salsa in controlled and field conditions.Crossref | GoogleScholarGoogle Scholar |
Wilmowicz E, Kęsy J, Kopcewicz J (2008) Ethylene and ABA interactions in the regulation of flower induction in Pharbitis nil. Journal of Plant Physiology 165, 1917–1928.
| Ethylene and ABA interactions in the regulation of flower induction in Pharbitis nil.Crossref | GoogleScholarGoogle Scholar | 18565620PubMed |
Wybouw B, De Rybel B (2018) Cytokinin a developing story. Trends in Plant Science 24, 177–185.
| Cytokinin a developing story.Crossref | GoogleScholarGoogle Scholar | 30446307PubMed |
Ye Q, Zhu W, Li L, Zhang S, Yin Y, Ma H, Wang X (2010) Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proceedings of the National Academy of Sciences of the United States of America 107, 6100–6105.
| Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development.Crossref | GoogleScholarGoogle Scholar | 20231470PubMed |
Yu H, Ito T, Zhao Y, Peng J, Kumar P, Meyerowitz EM (2004) Floral homeotic genes are targets of gibberellin signaling in flower development. Proceedings of the National Academy of Sciences of the United States of America 101, 7827–7832.
| Floral homeotic genes are targets of gibberellin signaling in flower development.Crossref | GoogleScholarGoogle Scholar | 15128937PubMed |
Yuan F, Guo J, Shabala S, Wang B (2018) Reproductive physiology of halophytes: current standing. Frontiers of Plant Science 9, 1954
| Reproductive physiology of halophytes: current standing.Crossref | GoogleScholarGoogle Scholar |
Zahir Z, Asghar H, Arshad M (2001) Cytokinin and its precursors for improving growth and yield of rice. Soil Biology & Biochemistry 33, 405–408.
| Cytokinin and its precursors for improving growth and yield of rice.Crossref | GoogleScholarGoogle Scholar |
Zeevaart JA (2008) Leaf-produced floral signals. Current Opinion in Plant Biology 11, 541–547.
| Leaf-produced floral signals.Crossref | GoogleScholarGoogle Scholar | 18691931PubMed |
Zhang D, Ren L, Yue J-h, Wang L, Zhuo L-h, Shen X-h (2014) GA4 and IAA were involved in the morphogenesis and development of flowers in Agapanthus praecox ssp. orientalis. Journal of Plant Physiology 171, 966–976.
| GA4 and IAA were involved in the morphogenesis and development of flowers in Agapanthus praecox ssp. orientalis.Crossref | GoogleScholarGoogle Scholar | 24913054PubMed |
Zhang YJ, Zhang Y, Zhang LL, Huang HY, Yang BJ, Luan S, Xue HW, Lin WH (2018) OsGATA7 modulates brassinosteroids‐mediated growth regulation and influences architecture and grain shape. Plant Biotechnology Journal 16, 1261–1264.
| OsGATA7 modulates brassinosteroids‐mediated growth regulation and influences architecture and grain shape.Crossref | GoogleScholarGoogle Scholar | 29345105PubMed |
Zheng C, Jiang D, Cai J, Dai T, Cao W (2010) Post-anthesis salinity and waterlogging and their combination affect uptake of potassium and sodium ions and starch accumulation in grain of wheat. Acta Ecologica Sinica 30, 4756–4764.
Zhu X, Liang W, Cui X, Chen M, Yin C, Luo Z, Zhu J, Lucas WJ, Wang Z, Zhang D (2015) Brassinosteroids promote development of rice pollen grains and seeds by triggering expression of Carbon Starved Anther, a MYB domain protein. The Plant Journal 82, 570–581.
| Brassinosteroids promote development of rice pollen grains and seeds by triggering expression of Carbon Starved Anther, a MYB domain protein.Crossref | GoogleScholarGoogle Scholar | 25754973PubMed |
