GA4 and IAA were involved in the morphogenesis and development of flowers in Agapanthus praecox ssp. orientalis

doi:10.1016/j.jplph.2014.01.012

Journal of Plant Physiology

Volume 171, Issue 11, 1 July 2014, Pages 966-976

https://doi.org/10.1016/j.jplph.2014.01.012 Get rights and content

Summary

The transition from vegetative to reproductive growth represents a major phase change in angiosperms. Hormones play important roles in this process. In this study, gibberellic acid (GA), cytokinins (CKs), indoleacetic acid (IAA), and abscisic acid (ABA) were analyzed during the flowering in Agapanthus praecox ssp. orientalis. Eleven types of endogenous gibberellins in addition to GA₁ were detected in various organs. GA₉ was detected with the highest concentrations, followed by GA₅, GA₈, and GA₁₉. However, GA₄ was the main bioactive GA that was involved in the regulation of flowering. Eight types of endogenous cytokinins were detected in A. praecox ssp. orientalis, and zeatin, zeatin riboside, zeatin-O-glucoside, and N⁶-isopentenyladenosine-5-monophosphate were present at higher levels throughout the study, of which zeatin plays an important role in the development of various organs. IAA increased by 581% in the shoot tips from the vegetative to inflorescence bud stages and had the most significant changes during flowering. Phytohormone immunolocalization analysis suggested that IAA involved in differentiation and development of each floral organs, GA and zeatin play important roles in floret primordia differentiation and ovule development. Using exogenous plant growth regulators proved that GA signaling regulate the scape elongation and stimulate early-flowering, and IAA signaling is involved in the pedicel and corolla elongation and delay flowering slightly.

Introduction

The transition from vegetative to reproductive growth represents a major phase change in angiosperms. Various environmental and endogenous signals that promote flowering induce an array of biochemical and cellular changes that alter the developmental fates of the shoot apical meristems (SAMs) (Zeevaart, 2008). Ultimately, the SAMs begin initiating floral primordia (FP) and generating the floral organs (Sablowski, 2007). Environmental factors often effect on hormone levels inducing plant flowering (Campos and Kerbauy, 2004). Phytohormones are endogenously occurring compounds that regulate multiple aspects of plant growth and development at low concentrations (Davies, 2004). Five classic phytohormones were described: gibberellic acid (GA), auxin, cytokinins (CKs), ethylene and abscisic acid (ABA). Recent advances have revealed that hormones are important regulators of inflorescence development (Barazesh and McSteen, 2008). GA has been implicated in the control of flowering in several species. In Arabidopsis, the severe reduction of endogenous GA delays flowering under long days and prevents flowering under short days (Blázquez et al., 1998). Eriksson et al. (2006) found that GA₄ is the active GA that is involved in the regulation of LFY transcription and Arabidopsis flowering time under short-day conditions, indicating that the GA pathway is the most important for floral induction under short days. Auxin and CKs have long been known to function in plant morphogenesis, Barazesh and McSteen (2008) indicated that the roles of hormones in inflorescence architecture are only beginning to be elucidated.

Agapanthus praecox spp. orientalis (Agapanthaceae) is a monocotyledonous, herbaceous, perennial plant. This species is characterized by a tuberous rootstock, fleshy tissues, a long flowering duration and large number of florets (Zhang et al., 2010), and often used as elegant cut flower and landscape plant. This plant is an excellent species for flowering study in monocot ornamental flowers. Sporogenesis, gametogenesis, embryology, and flowering bud anatomy were investigated in A. praecox ssp. orientalis (Zhang et al., 2010, Zhang et al., 2011a, Zhang et al., 2011b), and it was found that A. praecox ssp. orientalis flowering is not sensitive to photoperiods. However, temperature is the most important environmental factor for determining flower induction. In a previous study, we used transcriptomic and proteomic techniques to screen differentially expressed genes and proteins between the vegetative, induced, and reproductive buds; a transcription factors GAI (GA insensitive protein) that negatively regulates gibberellin signaling and auxin receptor protein TIR1 (Transport inhibitor response 1) were isolated, these gene expression pattern indicated that GA and auxin signaling plays an important role in regulating flowering development of A. praecox ssp. orientalis (Zhang et al., 2013). However, which aspects of flowering traits of Agapanthus are involved in GA and indole-acetic acid (IAA) signaling regulation are still unclear.

This paper aims, using a combination of phytohormone quantification and immunolocalization analyses, to reveal the hormones’ dynamic changes, metabolism rules, and biological regulatory functions during A. praecox ssp. orientalis flowering. This study will not only provide basic data for control blooming period and regulation of floral organs morphogenesis, but also can offer a better understanding for the future elucidation of flowering mechanisms in the genus Agapanthus.

Section snippets

Plant materials and growth conditions

Agapanthus praecox ssp. orientalis were grown at the Seedlings Practice Training Base of the Shanghai Vocational Technical College of Agriculture and Forestry in Shanghai, China (30°55′60′′ N, 121°71′46′′ E) at approximately 4 m above sea level. This site belongs to the warm temperate zone and maritime monsoon climate. Annual precipitation is 1254.9 mm. The maximum, minimum, and annual mean temperatures are 38.6 °C, −4.7 °C and 17.5 °C, respectively, and the annual sunshine duration is 1778.3 h (

Analysis of endogenous GAs

Endogenous GA₁, GA₃, GA₄, and their precursors and metabolites (Fig. 2a) were detected during flowering in A. praecox ssp. Orientalis. Eleven types of endogenous GAs in addition to GA₁ were detected in the stem tips, leaves, and roots. GA₉ was present in the highest concentrations, followed by GA₁₉, GA₅, and GA₈ (Fig. 2b and c).

In the stem tips, the GA₉ exhibited the highest concentrations and showed the largest range of fluctuation (2.60–37.92 ng g⁻¹ FW⁻¹), followed by GA₅, GA₈, GA₁₉, GA₄₄, and GA

Discussion

This is the first report of GAs and CKs from A. praecox ssp. orientalis. Eleven GAs and 8 CKs were identified in this study. GA₃ and GA₄ are bioactive gibberellin in all detected Gas and GA₄ is the main active GA regulating flower development of Agapanthus. GA₁ was not detected in A. praecox ssp. Orientalis. Instead, it was GA₈ as the metabolite of GA₁ which presented at high levels during flowering, suggesting almost all of GA₁ were converted to GA₈ by GA2ox. In A. praecox ssp. orientalis, the

Acknowledgments

This study received generous supports from the National Natural Science Foundation of China (Nos. 31170655 and 30872062), China Postdoctoral Science Foundation (2012M511099), Special Financial Grant from the China Postdoctoral Science Foundation (2013T60451), Key Projects of the Shanghai Agricultural Committee (2010-6-2), and Shanghai Graduate Education and Innovation Program (Horticulture).

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PhysiologyGA4 and IAA were involved in the morphogenesis and development of flowers in Agapanthus praecox ssp. orientalis

Summary

Introduction

Section snippets

Plant materials and growth conditions

Analysis of endogenous GAs

Discussion

Acknowledgments

Trends Plant Sci

J Plant Physiol

Curr Opin Plant Biol

Trends Plant Sci

Curr Opin Plant Biol

Plant Syst Evol

Agric Sci China

J Proteomics

Instructive roles for hormones in plant development

Int J Dev Biol

Gibberellin promote flowering of Arabidopsis by activating the LEAFY promoter

Plant Cell

Relationship between cellnumber, cell-size and fruit size of seeded fruits of tomato (Lycopersicon esculentum Mill), and those induced parthenocarpically by the application of plant-growth regulators

Plant Growth Regul

Quantitative analysis of cytokinins in plants by high performance liquid chromatography: electronspray ionization ion trap mass spectrometry

J Integr Plant Biol

Plant hormones: biosynthesis, signal transduction action!

Review the formation of adventitious roots: new concepts, new possibilities

In Vitro Cell Dev Biol Plant

Dynamics of cytokinins in apical shoot meristems of a day-neutral tobacco during floral transition and flower formation

Plant Physiol

GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation

Plant Cell

Abscisic acid signaling in seeds and seedlings

Plant Cell

Physiology
GA₄ and IAA were involved in the morphogenesis and development of flowers in Agapanthus praecox ssp. orientalis

GA₄ is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation