Os06g0196700

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OsARF16, an auxin response factor, functions in both auxin and −Pi responses in rice. [1]

Annotated Information

Function

Indole acetic acid (IAA) content, and expressions of auxin biosynthesis genes and auxin transporters in Nipponbare (NIP) and osarf16 under normal nutritional solution (CK), IAA and −Pi treatments. (from reference [1]).

OsARF16 effects on the −Pi signalling were correlated with auxin distribution To elucidate the function of ARF in rice, the structures of OsARF genes and OsARF12 features were investigated in our previous study [2][3] . Further identified and characterized the biological function of OsARF16 with TOS17 insertion in greater detail in rice. osarf16 mutant or Ov16 scarcely showed phenotypic differences in their roots, suggesting that OsARF16, one member of the ARF gene family might have functional redundancy with another member. However, the PR, LR, and RH of osarf16 showed auxin insensitivity, suggesting that OsARF16 plays a role on auxin response in root development. OsARF16 was mainly expressed in the stele and root tip of PR, AR and LR, which further supported that it was implicated in root development. And, OsARF16 expression in PR and LR was induced by auxin and −Pi treatments, and the expression of most OsLAX and OsPINs in osarf16 was markedly lower than in NIP under exogenous IAA treatment – this demonstrated that absence of OsARF16 might affect auxin polar transport. The temporal and spatial distribution of auxin mainly depends on the dynamic expression and subcellular localization of auxin efflux proteins, PINs [4]. The genomic sequencing of these auxin transporter genes, OsLAX and OsPINs, in rice was recently published in our study where it was compared to Arabidopsis [5], but their individual functions remain unknown. However, the expression pattern of OsARF16 in PR was the same as OsPIN1b, OsPIN4 and OsPIN9 [6], suggesting that OsARF16 may affect auxin transport mainly via these three genes. In addition, in osarf16 under −Pi, the expression of the four OsYUCCAs was highly induced, and most OsLAXs and OsPINs showed a similar trend with IAA treatment, indicating that an auxin transporter was also involved in −Pi response. The results indicated that −Pi response may alter auxin distribution or auxin polar transport via the regulation of OsARF16. In NIP, the auxin content was increased by −Pi condition while in osarf16 mutant, it was not affected. These results suggested that the impact of −Pi signalling on auxin distribution depends on OsARF16. On the other hand, in NIP, applying exogenous auxin enhanced Pi absorption, but in the OsARF16 knockout mutant, the Pi content was not increased. Therefore, the improvement of Pi absorption caused by changes of auxin distribution also depends on OsARF16. Taken together, results further confirmed that the effects of OsARF16 on −Pi signalling were correlated with auxin distribution.

Interaction between auxin distribution and −Pi signalling in Nipponbare (NIP) andosarf16. Indole acetic acid (IAA) contents from lateral roots (LR) initiation to maturation in NIP and osarf16 under CK and −Pi conditions. (from reference [1]).

Furthermore, microarray data [7][8] showed that auxin signalling takes part in differences responses to Pi deficiency in the shoot and root. Most of the auxin-induced genes in the rice root were also up-regulated by Pi deficiency. These data further confirmed that a number of genes co-participate in auxin and −Pi response, and not only OsARF16.

RH and LR development under P deficiency in rice depends on OsARF16-mediated −Pi signalling The phenotype of a plant under auxin treatment is similar to that for Pi starvation [9][10][11]. Our study found that osarf16 had auxin insensitivity and was also insensitive to Pi deficiency, especially in terms of RH and LR development. In NIP, but not in osarf16, the RH length was extended by −Pi, and OsARF16::GUS staining was also induced in RH by −Pi. RH development in −Pi has been infrequently reported [12][13][14]. The present study was the first to demonstrate that OsARF16 was a key regulator in RH expansion under −Pi in rice. Moreover, the LR number in osarf16 showed a small increase under −Pi, consistent with an arf19 mutant in Arabidopsis [15]. OsARF16 is highly homologous to ARF19, which is implicated in responses to Pi deficiency [16]. The data indicated that OsARF16 also acted in LR development under −Pi as well as ARF19. Plants respond to Pi deficiency by allocating more carbon to their roots, thereby increasing their root-to-shoot ratio [17][18]. The root-to-shoot ratio in osarf16 was only slightly increased compared with NIP, which further suggested that osarf16 was insensitive to Pi deficiency. It is worth mentioning that Fe accumulation in osarf16 under −Pi was lower than in NIP. A previous report showed that −Pi induced Fe acquisition and increased the Fe content of rice [19]. Our results suggested that the knockout of OsARF16 may indirectly affect the Fe signal via the −Pi response.

OsARF16 is an essential regulator in −Pi response

Indole acetic acid (IAA) content, and expressions of auxin biosynthesis genes and auxin transporters in Nipponbare (NIP) and osarf16 under normal nutritional solution (CK), IAA and −Pi treatments. (from reference [1]).

Under −Pi conditions, a plant enhances P absorption efficiency by regulating the expression of genes induced by phosphate starvation (PSIs) to maintain normal growth and development [20][21]. In Arabidopsis, the complete regulatory network for the P signal is important for plant responses to −Pi. Thus, the absence of AtPHR1 located in the centre of the P signal network resulted in the expression of numerous downstream genes that were inhibited under −Pi, and with an impaired P signal [22][23][24]. In rice, the knockdown of OsPHR2 led to a series of PSIs genes that were not distinctly induced by −Pi [25]. The genetic effect of OsARF16 knockout was similar to the absence of AtPHR1 and OsPHR2. The knockout of OsARF16 greatly weakened the transmission of the P signal, leading PSIs genes to lose their correct response. The P deficiency response still was impaired in the osarf16 mutant, even if OsPHR2 was normally expressed. Thus, the P deficiency response via OsPHR2 was dependent on OsARF16-mediated −Pi signalling. The effect of the OsPHR2 function was based on the normal expression of the OsARF16 gene, which maintained P signal transmission and allowed rice to respond to P deficiency in time.

In Arabidopsis, the modulation of auxin sensitivity by Pi depends on the auxin receptor transport inhibitor response1 (TIR1) and ARF19. Auxin sensitivity is enhanced in Pi-deprived plants by an increased expression of TIR1, which accelerates the degradation of AUX/IAA proteins. This indicated that ARF transcription factors activate/repress genes that are related to auxin signalling [26]. In rice, OsTIR1 in osarf16 was also less up-regulated by −Pi compared with NIP. Taken together, the results indicate that OsARF16 may be an essential regulator in −Pi response.

Mutation

Identification of mutant osarf16-Tos17 (osarf16) and phenotypic analysis. (from reference [1]).

Rice endogenous retrotransposon (TOS17) was integrated into the seventh exon of OsARF16 genes using analysis of the Rice Genome Resource Center (RGRC) database (http://www.rgrc.dna.affrc.go.jp) and sequencing. PCR analysis confirmed that the TOS17 fragment had been inserted into OsARF16 genes and the homozygous line was harvested. RT-PCR result demonstrated that OsARF16 was expressed in NIP and overexpressed in Ov16 and Ov16/mutant (Ov16/MT), but not the mutant osarf16. The phenotypes of NIP, osarf16, Ov16 and Ov16/MT were approximately the same under control (CK) conditions. However, the mutant osarf16 showed longer PR than the other three lines under IAA treatments, indicating it was insensitive to auxin. These results confirmed that OsARF16 was knocked out in osarf16, and that it rescued the function of OsARF16 in Ov16/MT. Exogenous auxin can decrease PR length [27] and induce LR formation [28] and RH elongation [29][30]. However, under IAA treatment, the PR length with 2,4-D and IBA treatments and the LR number in osarf16 were greater than NIP and Ov16, whereas the RH length in osaf16 was lower compared with both lines. Ov16 was more sensitive to IAA or NPA than NIP in terms of lateral root number. In addition, Ov16 was also more sensitive to IAA than NIP in terms of RH length, although the RH length in Ov16 under NPA treatment was similar to that of NIP. These results further confirmed that osarf16 is actually insensitive to auxin. Under IAA treatment, there was no difference in the adventitious root (AR) number between osarf16 and NIP, or Ov16, although more AR was produced in osarf16 than the other lines with an auxin influx transport inhibitor, that is, NOA treatment. To know the phenotype of osarf16 when blocking auxin transport, the PR length was measured under PATIs. The PR length in osarf16 was longer than NIP and Ov16 with TIBA, NPA and 1-NOA treatments, which indicated that osarf16 was also insensitive to PATIs. These results showed that OsARF16 was required for auxin responses in roots.


Expression

OsARF16 expression patterns. (from reference [1]).

The expression patterns of OsARF16 in various organs was evaluated using the GUS reporter gene. The 2641 bp of the OsARF16 sequence upstream of its ATG (predicted by the annotated rice genome (http://rice.plantbiology.msu.edu/cgi-bin/gbrowse/rice/#search) was fused to GUS and the transgene was introduced into rice NIP. Ten positive transgenic lines were obtained and three lines were used for further investigation. GUS staining was found to be prominent in the stele and root tip of PR and AR (equal to PR). In LR, OsARF16 was weakly expressed in the stele, root tip and primordia. OsARF16 was expressed at a lower level in the leaf relative to the leaf tip. It was not expressed in RH and it was highly expressed in the vascular tissue of the stem. OsARF16 expression was also observed in the anther, the stigma of the flower and the glume. Semi-quantitative RT-PCR (sqRT-PCR) further confirmed that OsARF16 was expressed at different levels in various tissues, consistent with the GUS staining results. Therefore, OsARF16 was expressed in different organs and tissues, with the highest expression being in roots and vasculature. The effects of auxin and −Pi treatments on the expression of OsARF16 was tested using the OsARF16::GUS reporter line. OsARF16 expression in the stele was completely inhibited by IAA, whereas that in the PR tip was highly induced by about 10-fold. OsARF16 expression in the stele, epidermis and tip of PR was highly induced (about 12-fold) by −Pi treatment. Interestingly, under the −Pi/+IAA treatment, the OsARF16 expression was highly increased in tip of PR than with only −Pi or IAA treatment (about 15-fold) while it was impaired in epidermis. This data provide an evidence for that auxin controls OsARF16 expression at a higher degree than −Pi. qRT-PCR analysis of PR further confirmed these trends. OsARF16::GUS staining was observed at the LR primordia, and induced by auxin and −Pi treatments. The above results suggest that the function of OsARF16 may be related to auxin and −Pi response.

OsARF16 expression pattern in root of Nipponbare (NIP; 7-day-old) under auxin and −Pi treatments. (from reference [1]).

Labs working on this gene

1. State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou 310058 2. State Key Laboratory of Rice Biology, China National Rice Research Institute, Chinese Academy of Agricultural Sciences, 359 Tiyuchang Road, Hangzhou, China

References

  1. ↑ 1.0 1.1 1.2 1.3 1.4 1.5 1.6 SHEN, C., WANG, S., ZHANG, S., XU, Y., QIAN, Q., QI, Y. and JIANG, D. A. (2013), OsARF16, a transcription factor, is required for auxin and phosphate starvation response in rice (Oryza sativa L.). Plant, Cell & Environment, 36: 607–620. doi: 10.1111/pce.12001
  2. ↑ Shen C., Wang S., Bai Y., Wu Y., Zhang S., Chen M., Guilfoyle T.J., Wu P. & Qi Y. (2010a) Functional analysis of the structural domain of ARF proteins in rice (Oryza sativa L. Journal of Experimental Botany 61, 3971–3981.
  3. ↑ Qi Y., Wang S., Shen C., Zhang S., Chen Y., Xu Y., Liu Y., Wu Y. & Jiang D. (2012) OsARF12, a transcription activator on auxin response gene, regulates root elongation and affects iron accumulation in rice (Oryza sativa). New Phytologist 193, 109–120.
  4. ↑ Bureau M., Rast M.I., Illmer J. & Simon R. (2010) JAGGED LATERAL ORGAN (JLO) controls auxin dependent patterning during development of the Arabidopsis embryo and root. Plant Molecular Biology 74, 479–491.
  5. ↑ Shen C., Bai Y., Wang S., Zhang S., Wu Y., Chen M., Jiang D. & Qi Y. (2010b) Expression profile of PIN, AUX/LAX and PGP auxin transporter gene families in Sorghum bicolor under phytohormone and abiotic stress. FEBS Journal 277, 2954–2969.
  6. ↑ Wang J.R., Hu H., Wang G.H., Li J., Chen J.Y. & Wu P. (2009b) Expression of PIN genes in rice (Oryza sativa L.): tissue specificity and regulation by hormones. Molecular Plant 2, 823–831.
  7. ↑ Jain M. & Khurana J.P. (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS Journal 276, 3148–3162.
  8. ↑ Zheng L., Huang F., Narsai R., et al. (2009) Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiology 151, 262–274.
  9. ↑ López-Bucio J., Cruz-Ramı'rez A. & Herrera-Estrella L. (2003) The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology 6, 280–287.
  10. ↑ Nacry P., Canivenc G., Muller B., Azmi A., Van O.H., Rossignol M. & Doumas P. (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiology 138, 2061–2074.
  11. ↑ Vanneste S. & Friml J. (2009) Auxin: a trigger for change in plant development. Cell 136, 1005–1016.
  12. ↑ Sánchez-Calderón L., López-Bucio J., Chacón-López A., Gutiérrez-Ortega A., Hernández-Abreu E. & Herrera-Estrella L. (2006) Characterization of low phosphorus insensitive mutants reveals a crosstalk between low phosphorus-induced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to phosphorus deficiency. Plant Physiology 140, 879–889.
  13. ↑ Bustos R., Castrillo G., Linhares F., Puga M.I., Rubio V., Pérez-Pérez J., Solano R., Leyva A. & Paz-Ares J. (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genetics 9, pii: e1001102.
  14. ↑ Wang X., Du G., Wang X., Meng Y., Li Y., Wu P. & Yi K. (2010b) The function of LPR1 is controlled by an element in the promoter and is independent of SUMO E3 Ligase SIZ1 in response to low Pi stress in Arabidopsis thaliana. Plant Cell and Physiology 51, 380–394.
  15. ↑ Pérez-Torres C.A., Lo'pez-Bucio J., Cruz-Ramı'rez A., Ibarra-Laclette E., Dharmasiri S., Estelle M. & Herrera-Estrella L. (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. The Plant Cell 20, 3258–3272.
  16. ↑ Wang D., Pei K., Fu Y., Sun Z., Li S., Liu H., Tang K., Han B. & Tao Y. (2007) Genome-wide analysis of the auxin response factor (ARF) gene family in rice (Oryza sativa). Gene 394, 13–24.
  17. ↑ López-Bucio J., Cruz-Ramı'rez A. & Herrera-Estrella L. (2003) The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology 6, 280–287.
  18. ↑ Hermans C., Hammond J.P., White P.J. & Verbruggen N. (2006) How do plants respond to nutrient shortage by biomass allocation? Trends in Plant Science 11, 610–617.
  19. ↑ Zheng L., Huang F., Narsai R., et al. (2009) Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiology 151, 262–274.
  20. ↑ Martín A.C., del Pozo J.C., Iglesias J., Rubio V., Solano R., de LaPeña A., Leyva A. & Paz-Ares J. (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. The Plant Journal 24, 559–567.
  21. ↑ Schachtman D.P. & Shin R. (2007) Nutrient sensing and signaling: NPKS. Annual Review of Plant Biology 58, 47–69.
  22. ↑ Rubio V., Linhares F., Solano R., Martín A.C., Iglesias J., Leyva A. & Paz-Ares J. (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes & Development 15, 2122–2133.
  23. ↑ Nilsson L., Müller R. & Nielsen T.H. (2007) Increased expression of the MYB-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana. Plant, Cell & Environment 30, 1499–1512.
  24. ↑ Panigrahy M., Rao D.N. & Sarla N. (2009) Molecular mechanisms in response to phosphate starvation in rice. Biotechnology Advances 27, 389–397.
  25. ↑ Zhou J., Jiao F., Wu Z., Li Y., Wang X., He X., Zhong W. & Wu P. (2008) OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiology 146, 1673–1686.
  26. ↑ Pérez-Torres C.A., Lo'pez-Bucio J., Cruz-Ramı'rez A., Ibarra-Laclette E., Dharmasiri S., Estelle M. & Herrera-Estrella L. (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. The Plant Cell 20, 3258–3272.
  27. ↑ Woodward A.W. & Bartel B. (2005) Auxin: regulation, action, and interaction. Annals of Botany 95, 707–735.
  28. ↑ Dong L., Wang L., Zhang Y., Zhang Y., Deng X. & Xue Y. (2006) An auxin-inducible F-box protein CEGENDUO negatively regulates auxin-mediated lateral root formation in Arabidopsis. Plant Molecular Biology 60, 599–615.
  29. ↑ Lee S.H. & Cho H.T. (2006) PINOID positively regulates auxin efflux in Arabidopsis root hair cells and tobacco cells. The Plant Cell 18, 1604–1616.
  30. ↑ Duan Q.H., Kita D., Li C., Cheung A.Y. & Wu H.M. (2010) FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proceedings of the National Academy of Sciences of the United States of America 107, 17821–11782.

Structured Information

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