Reduction of root flavonoid level and its potential involvement in lateral root emergence in Arabidopsis thaliana grown under low phosphate supply
Huixia Yang A B D , Hong Liu A B D , Gang Li C , Juanjuan Feng A B , Huanju Qin A , Xin Liu A , Hongwei Xue C and Daowen Wang A EA The State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Datun Road, Beijing 100101, China.
B Graduate School of Chinese Academy of Sciences, Yuquan Road, Beijing 100039, China.
C The State Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai 200032, China.
D These authors contributed equally to this work.
E Corresponding author. Email: dwwang@genetics.ac.cn
Functional Plant Biology 36(6) 564-573 https://doi.org/10.1071/FP08283
Submitted: 4 November 2008 Accepted: 25 March 2009 Published: 1 June 2009
Abstract
Although it is well known that phosphate (Pi) deficiency affects flavonoid accumulation in higher plants, knowledge on the regulation and potential function of flavonoids in the plants grown with low Pi supply is lacking. In this work, we found that low Pi treatment caused significant reduction of root flavonoid (e.g. quercetin, kaempferol and their derivatives) levels in both Columbia (Col-0) and Landsberg erecta (Ler) ecotypes of Arabidopsis thaliana (L.) Heynh. Further investigations revealed that the dysfunction of PHR1, PHO1, PHO2 and NPC4 did not affect the decrease of root flavonoid level by low Pi treatment. In contrast, pldζ2, a knockout mutant of the Arabidopsis phospholipase Dζ2, exhibited defects in the reduction of root flavonoid level and lateral root (LR) emergence under low Pi conditions. When grown under low Pi supply, the transport of auxin from the shoot apex into the root, expression of the auxin responsive DR5::GUS marker and induction of the auxin responsive genes were all significantly less efficient in pldζ2 than in wild-type (WT) control. This is the first report on the reduction of root flavonoid level and its likely contribution to increased LR emergence in Arabidopsis under Pi deficiency conditions, which may facilitate the adaptation of plants to the growth environments with poor Pi availability.
Additional keywords: kaempferol, phospholipase Dζ2, quercetin.
Acknowledgements
We thank Professor Bill Plaxton (Departments of Biology and Biochemistry, Queen’s University, Canada), Dr Jian Xu (Utrecht University, The Netherlands) and the anonymous reviewers for constructive comments on the manuscript. This work is supported by grants from the National Natural Science Foundation of China (30521001) and the Ministry of Science and Technology of China (2005CB120904).
Al-Ghazi Y,
Muller B,
Pinloche S,
Tranbarger TJ,
Nacry P,
Rossignol M,
Tardieu F, Doumas P
(2003) Temporal response of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signaling. Plant, Cell & Environment 26, 1053–1066.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Bariola PA,
MacIntosh GC, Green PJ
(1999) Regulation of S-like ribonuclease levels in Arabidopsis. Antisense inhibition of RNS1 or RNS2 elevates anthocyanin accumulation. Plant Physiology 119, 331–342.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Besseau S,
Hoffmann L,
Geoffroy P,
Lapierre C,
Pollet B, Legrand M
(2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. The Plant Cell 19, 148–162.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bhalerao RP,
Eklof J,
Ljung K,
Marchant A,
Bennett M, Sandberg G
(2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. The Plant Journal 29, 325–332.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bieleski RL
(1973) Phosphate pools, phosphate transport, and phosphate availability. Annual Review of Plant Physiology 24, 225–252.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Broun P
(2005) Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis. Current Opinion in Plant Biology 8, 272–279.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Brown DE,
Rashotte AM,
Murphy AS,
Normanly J,
Tague BW,
Peer WA,
Taiz L, Muday GK
(2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiology 126, 524–535.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Buer CS, Muday GK
(2004) The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. The Plant Cell 16, 1191–1205.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Burbulis IE,
Iacobucci M, Shirly BW
(1996) A null mutation in the first enzyme of flavonoid biosynthesis does not affect male fertility in Arabidopsis. The Plant Cell 8, 1013–1025.
|
CAS |
Crossref |
PubMed |
Casimiro I,
Marchant A,
Bhalerao RP,
Beeckman T, Dhooge S , et al.
(2001) Auxin transport promotes Arabidopsis lateral root initiation. The Plant Cell 13, 843–852.
|
CAS |
Crossref |
PubMed |
Cruz-Ramírez A,
Oropeza-Aburto A,
Razo-Hernández F,
Ramírez-Chávez E, Herrera-Estrella L
(2006) Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proceedings of the National Academy of Sciences of the United States of America 103, 6765–6770.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dai Y,
Wang H,
Li B,
Huang J,
Liu X,
Zhou Y,
Mou Z, Li J
(2006) Increased expression of MAP KINASE KINASE7 causes deficiency in polar auxin transport and leads to plant architectural abnormality in Arabidopsis. The Plant Cell 18, 308–320.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Debeaujon I,
Leon-Kloosterziel KM, Koornneef M
(2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiology 122, 403–414.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Delhaize E, Randall PJ
(1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiology 107, 207–213.
|
CAS |
PubMed |
Dixon RA, Pavia NL
(1995) Stress-induced phenylpropanoid metabolism. The Plant Cell 7, 1085–1097.
|
CAS |
Crossref |
PubMed |
Doerner P
(2008) Phosphate starvation signaling: a threesome controls systemic Pi homeostasis. Current Opinion in Plant Biology 11, 536–540.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Gaude N,
Nakamura Y,
Scheible W-R,
Ohta H, Dörmann P
(2008) Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. The Plant Journal 56, 28–39.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hamburger D,
Rezzonico E,
Petétot JM-C,
Somerville C, Poirier Y
(2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. The Plant Cell 14, 889–902.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hammond JP,
Broadley MR, White PJ
(2004) Genetic responses to phosphorus deficiency. Annals of Botany 94, 323–332.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Harborne J, Williams C
(2000) Advances in flavonoid research since 1992. Phytochemistry 55, 481–504.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Jacobs M, Rubery PH
(1988) Naturally-occurring auxin transport regulators. Science 241, 346–349.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Jain A,
Poling MD,
Karthikeyan AS,
Blakeslee JJ,
Peer WA,
Titapiwatanakun B,
Murphy AS, Raghothama KG
(2007) Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiology 144, 232–247.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lepiniec L,
Debeaujon I,
Routaboul JM,
Baudry A,
Pourcel L,
Nesi N, Caboche M
(2006) Genetics and biochemistry of seed flavonoids. Annual Review of Plant Biology 57, 405–430.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Li G, Xue HW
(2007) Arabidopsis PLDζ2 regulates vesicle trafficking and is required for auxin response. The Plant Cell 19, 281–295.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Li M,
Qin C, Wang XM
(2006a) Double knockouts of phospholipases Dzeta1 and Dzeta2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiology 140, 761–770.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Li M,
Welti R, Wang XM
(2006b) Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases Dζ1 and Dζ2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiology 142, 750–761.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Livak KJ, Schmittgen TD
(2001) Analysis of relative gene expression data using real time quantitative PCR and the 2ΔΔCt method. Methods 25, 402–408.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
López-Bucio J,
Hernández-Abreu E,
Sánchez-Calderón L,
Nieto-Jacobo MF,
Simpson J, Herrera-Estrella L
(2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiology 129, 244–256.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
López-Bucio J,
Hernández-Abreu E,
Sánchez-Calderón L,
Perez-Torres A,
Rampey RA,
Bartel B, Herrera-Estrella L
(2005) An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiology 137, 681–691.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mathesius U
(2008) Auxin: at the root of nodule development? Functional Plant Biology 35, 651–668.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Misson J,
Raghothama KG,
Jain A,
Jouhet J, Block MA , et al.
(2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proceedings of the National Academy of Sciences of the United States of America 102, 11934–11939.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Mo Y,
Nagel C, Taylor LP
(1992) Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proceedings of the National Academy of Sciences of the United States of America 89, 7213–7217.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Murphy A,
Peer WA, Taiz L
(2000) Regulation of auxin transport by aminopeptidase and endogenous flavonoids. Planta 211, 315–324.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Nacry P,
Canivenc G,
Muller B,
Azmi A,
Onckelen HV,
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Nakamura Y,
Awai K,
Masuda T,
Yoshioka Y,
Takamiya K, Ohta H
(2005) A novel phosphatidylcholine-hydrolyzing phospholipase C induced by phosphate starvation in Arabidopsis. The Journal of Biological Chemistry 280, 7469–7476.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Peer WA, Murphy AS
(2007) Flavonoids and auxin transport: modulators or regulators? Trends in Plant Science 12, 556–563.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Peer WA,
Brown DE,
Tague BW,
Muday GK,
Taiz L, Murphy AS
(2001) Flavonoid accumulation patterns of transparent testa mutants of Arabidopsis. Plant Physiology 126, 536–548.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Peer WA,
Bandyopadhyay A,
Blakeslee JJ,
Makam SN,
Chen RJ,
Masson PH, Murphy AS
(2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. The Plant Cell 16, 1898–1911.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Poirier Y,
Thoma S,
Somerville C, Schiefelbein J
(1991) Mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiology 97, 1087–1093.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Qin C, Wang X
(2002) The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLDzeta 1 with distinct regulatory domains. Plant Physiology 128, 1057–1068.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Raghothama KG
(1999) Phosphate acquisition. Annual Review of Plant Physiology and Plant Molecular Biology 50, 665–693.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Raghothama KG, Karthikeyan AS
(2005) Phosphate acquisition. Plant and Soil 274, 37–49.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Reed RC,
Brady SR, Muday GK
(1998) Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiology 118, 1369–1378.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Routaboul JM,
Kerhoas L,
Debeaujon I,
Pourcel L,
Caboche M,
Einhorn J, Lepiniec L
(2006) Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana. Planta 224, 96–107.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Rubio V,
Linhares F,
Solano R,
Martín AC,
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Sánchez-Calderón L,
López-Bucio J,
Chacón-López A,
Cruz-Ramírez A,
Nieto-Jacobo F,
Dubrovsky JG, Herrera-Estrella L
(2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant & Cell Physiology 46, 174–184.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schachtman DP, Shin R
(2007) Nutrient sensing and signaling: NPKS. Annual Review of Plant Biology 58, 47–69.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Springob K,
Nakajima JI,
Yamazaki M, Saito K
(2003) Recent advances in the biosynthesis accumulation of anthocyanins. Natural Product Reports 20, 288–303.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Stewart AJ,
Chapman W,
Jenkins GI,
Graham I,
Martin T, Crozier A
(2001) The effect of nitrogen and phosphorus deficiency on flavonol accumulation in plant tissues. Plant, Cell & Environment 24, 1189–1197.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Taylor LP, Grotewold E
(2005) Flavonoids as developmental regulators. Current Opinion in Plant Biology 8, 317–323.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Tian Q,
Uhlir NJ, Reed JW
(2002) Arabidopsis SHY2/IAA3 inhibits auxin-regulated gene expression. The Plant Cell 14, 301–319.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ticconi CA,
Delatorre CA,
Lahner B,
Salt DE, Abel S
(2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. The Plant Journal 37, 801–814.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ulmasov T,
Murfett J,
Hagen G, Guilfoyle TJ
(1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. The Plant Cell 9, 1963–1971.
|
CAS |
Crossref |
PubMed |
Vance CP,
Uhde-Stone C, Allan DL
(2003) Phosphorus acquisition and use: critical adaptations by plants securing a nonrenewable resource. New Phytologist 157, 423–447.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Winkel-Shirley B
(2002) Biosynthesis of flavonoid and effects of stress. Current Opinion in Plant Biology 5, 218–223.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Winkel-Shirley B,
Kubasek WL,
Storz G,
Bruggemann E,
Koornneef M,
Ausubel FM, Goodman HM
(1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. The Plant Journal 8, 659–671.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Xie DY,
Sharma SB,
Paiva NL,
Ferreira D, Dixon RA
(2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 299, 396–399.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |