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Arabidopsis Cryptochrome 1 Functions in Nitrogen Regulation of Flowering

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Arabidopsis Cryptochrome 1 Functions in Nitrogen Regulation of Flowering Arabidopsis cryptochrome 1 functions in nitrogen regulation of flowering Shu Yuana,b,1,2, Zhong-Wei Zhangb,1, Chong Zhenga,1, Zhong-Yi Zhaoa,c,1, Yu Wanga,1, Ling-Yang Fengb, Guoqi Niua, Chang-Quan Wangb, Jian-Hui Wangd, Hong Fenge, Fei Xuf, Fang Baoa, Yong Hua, Ying Caoa, Ligeng Maa, Haiyang Wangg, Dong-Dong Kongh, Wei Xiaoa, Hong-Hui Linc, and Yikun Hea,2 aCollege of Life Science, Capital Normal University, Beijing 100048, China; bCollege of Resources Science and Technology, Sichuan Agricultural University, Chengdu 611130, China; cMinistry of Education Key Laboratory for Bio-Resource and Eco-Environment, College of Life Science, Sichuan University, Chengdu 610064, China; dHorticulture Institute, Sichuan Academy of Agricultural Sciences, Chengdu 610066, China; eSchool of Life Sciences, Chengdu Normal College, Chengdu 611130, China; fCenter of Applied Biotechnology, Wuhan Institute of Bioengineering, Wuhan 430415, China; gBiotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China; and hDepartment of Chemistry, Capital Normal University, Beijing 100048, China Edited by Xing Wang Deng, Peking University, Beijing, China, and approved May 26, 2016 (received for review February 5, 2016) The phenomenon of delayed flowering after the application of GI and CO are regulated by the circadian clock and by light sig- nitrogen (N) fertilizer has long been known in agriculture, but the naling simultaneously and at both transcriptional and post- detailed molecular basis for this phenomenon is largely unclear. transcriptional levels, to ensure the transcription of FT under LD Here we used a modified method of suppression-subtractive hybrid- conditions, but not under SD conditions (10). ization to identify two key factors involved in N-regulated flowering Nitrogen (N) availability is one of the key factors controlling + time control in Arabidopsis thaliana, namely ferredoxin-NADP -oxi- developmental and growth to ensure plant survival and reproduction doreductase and the blue-light receptor cryptochrome 1 (CRY1). The (11). Arabidopsis, like other plants, flowers earlier under low-nitrate expression of both genes is induced by low N levels, and their loss-of- conditions (11). Previous studies have reported that the flowering function mutants are insensitive to altered N concentration. Low-N activators CO, FT, LEAFY (LFY), and APETALA1 (AP1) are + conditions increase both NADPH/NADP and ATP/AMP ratios, which induced, but the flowering repressor FLC (FLOWERING LOCUS in turn affect adenosine monophosphate-activated protein kinase C) is repressed in low-nitrate conditions (12, 13). There are also (AMPK) activity. Moreover, our results show that the AMPK activity reports that nitrate availability controls the GA pathway at different and nuclear localization are rhythmic and inversely correlated with levels (GA biosynthesis, perception, and signaling) to influence the nuclear CRY1 protein abundance. Low-N conditions increase but timing of vegetative to reproductive phase change (13, 14). However, high-N conditions decrease the expression of several key compo- Castro Marín et al. (15) showed that low nitrate induced flowering CCA1 LHY TOC1 nents of the central oscillator (e.g., , ,and )andthe by a pathway downstream of the floral integrators and independent GI CO flowering output genes (e.g., and ). Taken together, our results of photoperiod, GA, and autonomous pathways. Thus, the de- suggest that N signaling functions as a modulator of nuclear CRY1 tailed molecular mechanisms, especially the key factors to sense protein abundance, as well as the input signal for the central circa- and transmit the N signal to regulate flowering remain elusive. dian clock to interfere with the normal flowering process. In this study, we used a modified method of suppression- PLANT BIOLOGY subtractive hybridization (SSH) to identify two key factors adenosine monophosphate-activated protein kinase | circadian clock | + involved in N-regulated flowering: ferredoxin-NADP -oxidore- cryptochrome 1 | ferredoxin-NADP+-oxidoreductase 1 | ductase (FNR1) (16) and the blue-light photoreceptor crypto- nitrogen-regulated flowering chrome 1 (CRY1) (17). Their loss-of-function mutants are he transition from vegetative to reproductive development is Significance Ta central event in the plant life cycle, which is coordinately regulated by various endogenous and external cues. In the model Overapplication of nitrogen (N) fertilizer causes delayed flowering dicotyledonous plant species Arabidopsis thaliana, five distinct and negatively impacts the function and composition of natural genetic pathways regulating flowering time have been established: ecosystems and climate. In this study, we demonstrate that flow- the vernalization pathway, photoperiod pathway, gibberellin acid ering time variations regulated by altered nitrogen levels are me- + (GA) pathway, autonomous pathway, and endogenous (age) diated by two key factors: ferredoxin-NADP -oxidoreductase (FNR1) pathway (1). These pathways ultimately converge to regulate a and the blue-light receptor cryptochrome 1 (CRY1). Nitrogen regu- set of floral integrator genes, FLOWERING LOCUS T (FT) and lates FNR1 expression, thereby contributing to changes in NADPH/ SUPPRESSOR OF CONSTANS 1 (SOC1), which in turn activate NADP+ and ATP/AMP ratios, which in turn activates adenosine the expression of floral meristem identity genes to trigger the monophosphate-activated protein kinase to modulate nuclear CRY1 formation of flowers (2–4). abundance, which further acts in the N signal input pathway to Plants use the circadian clock as the timekeeping mechanism affect central clock function and flowering time. A better un- to measure day length and to ensure flowering at the proper season derstanding of N-regulated floral transition will offer bio- (5, 6). As a facultative long-day (LD) plant, Arabidopsis flowers technological solutions to improve sustainable agriculture. earlier under LD conditions than under short-day (SD) conditions. Forward genetics in A. thaliana have identified the GI-CO-FT hi- Author contributions: S.Y. and Y. He designed research; S.Y., Z.-W.Z., C.Z., Z.-Y.Z., Y.W., erarchy as the canonical genetic pathway promoting flowering L.-Y.F., and G.N. performed research; S.Y., C.-Q.W., J.-H.W., H.F., F.X., F.B., Y. Hu, Y.C., L.M., H.W., D.-D.K., and H.-H.L. analyzed data; and S.Y., H.W., D.-D.K., W.X., and Y. He specifically under LD conditions (5, 7, 8). In this pathway, GI wrote the paper. (GIGANTEA) can be considered the output point of the circadian The authors declare no conflict of interest. clock to control flowering by regulating CONSTANS (CO)ex- This article is a PNAS Direct Submission. pression in the right phase, which activates expression of FT and 1S.Y., Z.-W.Z., C.Z., Z.-Y.Z., and Y.W. contributed equally to this work. TSF (TWIN SISTER OF FT) in the companion cells of the phloem 2To whom correspondence may be addressed. Email: [email protected] or yhe@ within the vascular tissue (2, 9). FT and TSF proteins act as the cnu.edu.cn. long-sought florigens that move from leaves to the apical meristem This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. to induce genes required for reproductive development (2–4). Both 1073/pnas.1602004113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1602004113 PNAS | July 5, 2016 | vol. 113 | no. 27 | 7661–7666 Downloaded by guest on September 30, 2021 Fig. 1. Procedures, schematic diagram of the SSH screens, and results. (A) Experimental procedure for SSH. (B) Schematic diagram of two-round SSH. Red circles indicate floral transition-induced genes, which can be further induced by 1/20 LN conditions (red disk); blue circles indicate LN-induced genes, which can be further induced after floral transition (blue disk). Purple disks indicate genes expressed only at 1/20 LN conditions and after floral transition (two-condition synergistic genes). (C) PCR verification of first-round and second-round SSH. insensitive to altered N levels. We show that N regulates FNR1 at seventh day, in NN after floral transition at the 13th day, in LN + the transcription level, thus affecting ratios of NADPH/NADP before floral transition at the seventh day, and in LN after floral and ATP/AMP, which in turn affect adenosine monophosphate- transition at the 11th day. Pairwise comparison of these samples activated protein kinase (AMPK) activity and nuclear CRY1 pro- through two rounds of SSH screens (Fig. 1) revealed that genes tein abundance. Our data imply that the nuclear level of CRY1 encoding FNR1 and CRY1 are prominently enriched in both functions as an input cue to regulate the amplitude of circadian final results (SI Appendix, Tables S1 and S2). Induction of FNR1 clock transcripts, thereby controlling flowering time. and CRY1 gene expression by LN (increased by 5.2-fold for FNR1 andby4.8-foldforCRY1) was further confirmed by quan- Results titative RT-PCR (SI Appendix,Fig.S3). Statistical analysis revealed Identification of FNR1 and CRY1 as N-Responsive Genes. Earlier that the abundance of FNR1 and CRY1 transcript is negatively microarray studies have shown that thousands of Arabidopsis correlated with flowering time (P < 0.05), implying that FNR1 and genes (∼7% of the Arabidopsis transcriptome) are N-responsive CRY1 act as two positive regulators of N-regulated flowering. (18). To search for key factors involved in N-regulated flowering, Furthermore, the FNR1 expression can be induced by high-Fe we performed a modified SSH screen with Arabidopsis seedlings and S conditions (0.4 mM FeSO4·7H2O in the MS medium) and grown on media containing different levels of N. We first de- CRY1 expression can be induced by blue-light treatment (SI termined the appropriate N treatment levels and Arabidopsis Appendix, Fig. S3), in disagreement with previous reports (17, floral transition times. When grown at reduced N levels (1/20 N, 19) but consistent with reported transcriptome analyses (20, 21). NH4NO3, and KNO3 equally reduced), the flowering time was shortened from to 21 d from 25 d when grown on normal-N Arabidopsis fnr1 and cry1 Mutants Are Insensitive to N Changes.
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