Abstract
Nutrition affects plant growth and development, including flowering. Flowering represents the transition from the vegetative period to the reproduction period and requires the consumption of nutrients. Moreover, nutrients (e.g., nitrate) act as signals that affect flowering. Regulation of flowering time is therefore intimately associated with both nutrient-use efficiency and crop yield. Here, we review current knowledge of the relationships between nutrients (primarily nitrogen, phosphorus, and potassium) and flowering, with the goal of deepening our understanding of how plant nutrition affects flowering.
1 Introduction
Plants must acquire at least 14 essential mineral elements for their growth, development, structure, physiology, and reproduction; these comprise both macronutrients and micronutrients (). Nutrient availability is tightly linked to flowering time, which requires resources for producing and sustaining sink tissues for reproduction (). Deficiency or excess of nutrients results in a stress response that affects flowering time (; ; ). Flowering time control integrates external environmental factors (daylength, temperature, light, stress, and nutritional status) and endogenous signals from the plant itself (; ; ). The mechanisms by which several environmental factors (daylength, temperature, and stress) alter flowering time have been well characterized and reviewed (; ; ; ; ; ; ; ); however, there are fewer reports on how nutrients affect flowering time. In this review, we summarize what is known about the interactions between nutrients [primarily nitrogen (N), phosphorus (P), and potassium (K)] and flowering time. Genes previously reported to be involved in nutrient-mediated modulation of flowering time are summarized in Table 1.
Table 1
| Species | Gene name | Nutrient | Effect | Reference |
|---|---|---|---|---|
| Arabidopsis | NRT1.1 | Nitrogen | Floral promotion | (; ) |
| FNR1 | Nitrogen | Floral promotion (1.47 mM N, 29.4 mM N), floral inhibition (117.6 mM N) | (Yuan et al., 2016) | |
| CRY1 | Nitrogen | Floral promotion (1.47 mM N) | (Yuan et al., 2016) | |
| miR172 | Nitrogen | Floral promotion | () | |
| DELLA | Nitrogen | Floral inhibition | () | |
| SMZ/SNZ | Nitrogen | Floral inhibition (3 mM KNO3) | () | |
| SMZ/SNZ/TOE1/TOE2 | Nitrogen | Floral inhibition (1 mM KNO3, 3 mM KNO3) | () | |
| FT | Nitrogen | Floral promotion (1 mM KNO3, 3 mM KNO3) | () | |
| SOC1 | Nitrogen | Floral promotion (1.25 mg N, 31.5 mg N) | () | |
| NLP6 | Nitrogen | Floral promotion (31.5 mg N, short day) | () | |
| NLP7 | Nitrogen | Floral promotion (31.5 mg N) | () | |
| NLP6/NLP7 | Nitrogen | Floral promotion (31.5 mg N) | () | |
| FBH4 | Nitrogen | Floral promotion (0.3 mM N, 3 mM N) | () | |
| Rice | NRT1.1a | Nitrogen | Floral promotion | (Wang et al., 2018) |
| NHD1 | Nitrogen | Floral promotion (0.25 mM N, 2.5 mM N; 90, 180, and 360 kg N/ha) | (Zhang et al., 2021) | |
| HD3a | Nitrogen | Floral promotion (180 and 360 kg N/ha) | (Zhang et al., 2021) | |
| DREB1c | Nitrogen | Floral promotion | (Wei et al., 2022) | |
| Arabidopsis | NLA | Phosphorus | Floral inhibition | () |
| PHF1 | Phosphorus | Floral promotion | () | |
| miR399 | Phosphorus | Floral promotion | () | |
| PHO2 | Phosphorus | Floral inhibition | () | |
| Wheat | PSTOL | Phosphorus | Floral inhibition | () |
| Apple | MYB2 | Phosphorus | Floral inhibition | (Yang et al., 2020) |
| Arabidopsis | AKT2 | Potassium | Floral promotion | () |
| CBL4 | Potassium | Floral promotion | () | |
| CIPK6 | Potassium | Floral promotion | () | |
| NaKR1 | Potassium | Floral promotion (long-day) | (Zhu et al., 2016) | |
| SPL3 | Potassium | Floral inhibition | () |
Genes involved in nutrient-mediated modulation of flowering time.
2 Nutrients and flowering time
2.1 Nitrogen
Nitrogen (N) is the most important macronutrient for plant growth, needed for proper root morphology, shoot growth, stomatal opening, flowering, yield, and senescence (; ; ; ; ; Wei et al., 2022; Zinta et al., 2022). The influence of N on flowering time in Arabidopsis and rice can be visualized as a U-shaped trend (; ; Zhang et al., 2021), with both deficiency and sufficiency of N postponing flowering time.
The first evidence that nitrate is involved in the regulation of flowering time in Arabidopsis was obtained from genetic studies showing that nia1nia2 mutants flower later than their wild-type controls (; ). Nitrate regulates the expression of flowering-related genes at the shoot apical meristem (SAM) to modulate flowering time; these genes include SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1), CONSTANS (CO), FLOWERING LOCUS C (FLC), LEAFY (LFY), APETALA1 (AP1), and FLOWERING LOCUS T (FT) (; ). NIN-LIKE PROTEIN6 (NLP6) and NLP7 function in the regulation of signaling by binding to the promoter of SOC1-LIKE3 (SPL3) and SPL5 in the Arabidopsis SAM (; ; ). Nitrate greatly affects the vegetative growth of plants, so defining whether it has a direct influence on flowering is difficult (; ). To separate the effects of nitrate on growth and flowering, a growth system using glutamine supplementation was established; low nitrate was still found to accelerate flowering in late-flowering Arabidopsis mutants with impaired photoperiod, temperature, GA, and autonomous flowering pathways (; Weber and Burow, 2018), suggesting that regulates flowering time independently of the autonomous, light, and gibberellin pathways in Arabidopsis (). Moreover, delayed flowering time in co, ft, fd (FLOWERING LOCUS D), and tsf (TWIN SISTER OF FT) mutants as well as plants overexpressing microRNA156 (miR156) under low-N conditions proves that -dependent flowering is indeed independent of age and photoperiod pathways (; ). These observations indicate that -dependent flowering pathways are dependent on the concentration and source of nitrate used (KNO3, NH4NO3, mixed, or supplemented with glutamine) (; ).
Protein phosphorylation is important for the transmission of information regarding N availability (; ; ; ; ). Notably, reported that the phosphorylation state of FLOWERING BHLH4 (FBH4) is altered by changes in N conditions, clarifying a link between N availability and the regulation of flowering. The kinase activity of SNF1-RELATED KINASE1 (SnRK1) is inhibited under low-N concentrations, resulting in a decrease in the phosphorylation of its direct target, FBH4 (). This in turn promotes nuclear localization of FBH4, increasing the transcription of the flowering time genes CO and FT ().
Delaying flowering by applying N fertilizers to crops is common in agricultural production, but the underlying molecular mechanism of this delay is largely unclear. High N delays flowering by improving transcription levels of SCHNARCHZAPFEN (SNZ) and SCHLAFMUTZE (SMZ), which directly bind to the promoter of FT (; ). Mutants lacking ferredoxin–NADP oxidoreductase (FNR1) flower later than wild-type plants, and fnr1 and cryptochrome1 (cry1) mutants display insensitivity to different levels of N at flowering time (Yuan et al., 2016). FNR1 is inhibited at high N levels, leading to upregulation of CRY1 and degradation of FNR1 in the nucleus, thereby reducing transcript levels of central circadian clock genes [e.g., TOC1 (TIMING OF CAB EXPRESSION1), CCA1 (CIRCADIAN CLOCK-ASSOCIATED1), and LHY (LATE ELONGATED HYPOCOTYL)] and some flowering-output genes [e.g., GIGANTEA (GI) and CO] to disturb the flowering process (; Yuan et al., 2016). N signaling therefore alters the abundance of CRY1 protein and is also involved in the pathway of the central circadian clock, which regulates flowering.
Breeding programs often aim to develop cultivars that tolerate high N inputs without delayed flowering. OsNRT1.1A increases N utilization without delaying flowering, offering potential for the development of crops with the combined traits of early maturation and high yield (Wang et al., 2018). Rice, a short-day plant, has special flowering pathways besides the conserved flowering genes shared with long-day plants, such as Arabidopsis (; ). Arabidopsis and other upland plants prefer to absorb N as nitrate, while paddy rice prefers ammonium (); hence, these species use different mechanisms for regulating flowering time in response to N forms and concentration. (Zhang et al., 2021) showed that N-mediated heading date1 (Nhd1), which shares a high sequence similarity with CCA1 and LHY, increases the levels of florigen Hd3a to control flowering time but downregulates Fd-GOGAT for N assimilation in rice. Recent studies have shown that transcription of OsDREB1C (dehydration-responsive element binding) is induced by light and low N, suggesting a function in N-use efficiency and flowering time (Wei et al., 2022). Plants lacking this gene display delayed flowering under long-day conditions because OsDREB1C binds to the exons of OsFTL1, activating its transcription (Wei et al., 2022). As orthologs of Nhd1 or DREB exist in other crops, the functions of Nhd1 and DREB in the regulation of flowering and N-use efficiency should be useful in other crops (Wei et al., 2022).
2.2 Phosphorus
Plants obtain phosphorus (P) mainly in the form of inorganic phosphate (Pi) (). Low Pi availability generally delays flowering time in annual plants (; ); for example, the nla (NITROGEN LIMITATION ADAPTATION) mutant accumulates high levels of Pi and flowers significantly earlier than the wild type, while phf1 (PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1) mutant with lower Pi accumulation flowers later than the wild type (). MiR399 and PHOSPHATE2 (PHO2) are known to play a role in the maintenance of Pi homeostasis, and miR399b-overexpressing plants and pho2 mutant accumulate high levels of Pi and exhibit early flowering phenotype via upregulation of TSF (; ). Moreover, the overexpression of TaPSTOL in transgenic wheat showed a significantly lower physiological P use efficiency and the P efficiency ratio than the wild type and were significantly later in flowering than the wild type, which revealing that P has a significant effect on flowering time (). Transgenic expression of the Pi-responsive gene MdMYB2 postpones flowering in Arabidopsis by decreasing the transcription of flowering genes (CO, SOC1, LFY, and FT) (Yang et al., 2020). No further data are available regarding the molecular mechanisms by which Pi availability affects flowering in crops such as rice, maize (Zea mays), and soybean (Glycine max); thus, further work is required to understand these processes in crop plants.
Phenological delay under low-Pi conditions is beneficial because it gives plants more time for P absorption (). By contrast, plants generally flower early to complete their life cycles more quickly under low-N conditions (). Notably, crosstalk between N and P shows their accumulated influence on flowering (; Yang et al., 2020). MiR827 and NLA regulate Pi homeostasis in a N-dependent manner (), and availability of both N and Pi affects flowering time by altering the expression of FLC, CO, FT, LFY, AP1, and some downstream genes of miR156–SPL (; Vidal et al., 2014; ). The mechanisms by which N and P affect flowering time are worthy of further study, especially in crops.
2.3 Potassium
The concentration of potassium ions (K+) in plant cells can be as high as 100 mM, but the concentration in soil is only 100–1000 μM (; Wang and Wu, 2015; Wang et al., 2021). Absorption of K+ through roots requires K+ channels and transporters (Wang et al., 2021). In Arabidopsis, loss of AKT2/3 (Arabidopsis K+ channel) changes the flowering time phenotype, implying that, similar to N and P, K+ availability also affects flowering time (); however, the molecular mechanisms involved are not clear. Additional studies report that akt2, cbl4 (calcineurin B-like proteins), and cipk6 exhibit analogous late flowering under short-day treatment (), indicating that regulation of ion channels involved in the flowering pathway and the activity of K+ channels are modulated via a Ca2+ sensor kinase (). () found that mutant plants lacking SODIUM POTASSIUM ROOT DEFECTIVE1 (NaKR1) over-accumulate Na+ and K+ and display late flowering. NaKR1 participates in the phloem transport of FT protein (Zhu et al., 2016) and increases the transcription level of FT under long-day treatment, dependent on K+ concentration. NaKR1 therefore regulates not only florigen production, but also transport (). It is thus clear that the miR156–SPL module might respond to N, P, and K, which deserves more in-depth study.
3 Perspective
Besides N, P, and K, there are at least 11 essential nutrients required by plants. Whether and how these nutrients affect flowering time require further exploration. (Yuan et al., 2016) suggested that FNR1 promotes flowering in response to N, and the level of FNR1 is also induced by sufficient iron (Fe) and sulfur (S) supply. Therefore, Fe and S may also regulate plant flowering time through FNR1. Recent studies have mainly focused on the absorption, translocation, and reuse of nutrients (; Wani et al., 2021; ; ; ; ; ; ; ; ; Xie et al., 2022), meaning that the potential mechanisms underlying nutrient-regulated flowering remain largely unknown in plants, especially crops. UV stress, drought, salt, cold, and heat also alter flowering (; ; ; ; ). Improving nutrient-use efficiency by coordinating flowering time is an effective way to increase crop yield; thus, the effects of interaction between flowering time and nutrients on crop yield are in need of more in-depth study.
Statements
Author contributions
YZ and LC wrote this mini review, BL revised the mini review, FK and LC conceived the review. All authors contributed to the article and approved the submitted version.
Funding
This work was funded by the National Natural Science Foundation of China (32001502, 31901499), and also supported by the China Postdoctoral Science Foundation (2019M652839, 2020M682655).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
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Summary
Keywords
nutrient, flowering time, nitrogen, phosphorus, potassium
Citation
Zhang Y, Liu B, Kong F and Chen L (2023) Nutrient-mediated modulation of flowering time. Front. Plant Sci. 14:1101611. doi: 10.3389/fpls.2023.1101611
Received
18 November 2022
Accepted
05 January 2023
Published
19 January 2023
Volume
14 - 2023
Edited by
Gaetano Distefano, University of Catania, Italy
Reviewed by
Yongqiang Zhang, Fujian Agriculture and Forestry University, China
Updates
Copyright
© 2023 Zhang, Liu, Kong and Chen.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Liyu Chen, chenliyu1715@gzhu.edu.cn; Fanjiang Kong, kongfj@gzhu.edu.cn
This article was submitted to Crop and Product Physiology, a section of the journal Frontiers in Plant Science
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