- Research article
- Open Access
BYPASS1: synthesis of the mobile root-derived signal requires active root growth and arrests early leaf development
© Van Norman et al; licensee BioMed Central Ltd. 2011
Received: 14 May 2010
Accepted: 3 February 2011
Published: 3 February 2011
The Arabidopsis bypass1 (bps1) mutant root produces a biologically active mobile compound that induces shoot growth arrest. However it is unknown whether the root retains the capacity to synthesize the mobile compound, or if only shoots of young seedlings are sensitive. It is also unknown how this compound induces arrest of shoot growth. This study investigated both of these questions using genetic, inhibitor, reporter gene, and morphological approaches.
Production of the bps1 root-synthesized mobile compound was found to require active root growth. Inhibition of postembryonic root growth, by depleting glutathione either genetically or chemically, allowed seedlings to escape shoot arrest. However, the treatments were not completely effective, as the first leaf pair remained radialized, but elongated. This result indicated that the embryonic root transiently synthesized a small amount of the mobile substance. In addition, providing glutathione later in vegetative development caused shoot growth arrest to be reinstated, revealing that these late-arising roots were still capable of producing the mobile substance, and that the older vegetative leaves were still responsive.
To gain insight into how leaf development responds to the mobile signal, leaf development was followed morphologically and using the CYCB1,1::GUS marker for G2/M phase cells. We found that arrest of leaf growth is a fully penetrant phenotype, and a dramatic decrease in G2/M phase cells was coincident with arrest. Analyses of stress phenotypes found that late in development, bps1 cotyledons produced necrotic lesions, however neither hydrogen peroxide nor superoxide were abundant as leaves underwent arrest.
bps1 roots appear to require active growth in order to produce the mobile bps1 signal, but the potential for this compound's synthesis is present both early and late during vegetative development. This prolonged capacity to synthesize and respond to the mobile compound is consistent with a possible role for the mobile compound in linking shoot growth to subterranean conditions. The specific growth-related responses in the shoot indicated that the mobile substance prevents full activation of cell division in leaves, although whether cell division is a direct response remains to be determined.
Plants synthesize a wide array of metabolites, and a major goal of metabolomics is to identify natural plant metabolites and their associated functions (reviewed in [1–3]). Recent advances facilitating identification of metabolites [4, 5] have led to identification of groups of metabolites that correlate with important plant traits, such as growth rate and biomass [6, 7], and identified metabolic regulators such as leucine . However, how specific metabolites other than characterized hormones function in signaling and development is largely unknown. One approach to learning about alternate signaling molecules is to study mutants with signaling-related defects.
The Arabidopsis bypass1 (bps1) mutant might be an important tool for identifying a metabolite functioning as a long-distance signal. The bps1 mutant produces small abnormal roots and shoot development arrests soon after germination. This phenotype is linked to a mobile substance as the bps1 mutant root is necessary to induce arrest of bps1 shoots, and in graft chimeras, the bps1 root is sufficient to induce arrest of the wild-type shoot . These observations led to a model featuring BPS1 as a negative regulator that was required to prevent the excess production of a mobile substance. The mobile compound appears to be novel, and its synthesis requires carotenoid biosynthesis . The pathway producing the bps1 mobile compound appears to be conserved in plant lineages, as knock-downs of conserved BPS-like genes in tobacco produced similar phenotypes . Critical questions include whether this mobile compound is an endogenous developmental regulator, and how it modifies shoot growth.
Control over shoot branching by a root-derived signal has been elegantly analyzed in pea, rice, and Arabidopsis [12–15]. In these systems, mutations disrupting biosynthetic enzymes lead to reduced production of a mobile compound that controls auxin transport in the shoot [16, 17]. Recently, this substance was identified as strigolactone [18, 19]. Additional unknown root-to-shoot signals have been implicated by studies of drought (reviewed in ), soil compaction , nutrient depletion [22–24] and low-fluence UV-B light . The identities of the mobile compounds elicited by these treatments are unknown; it is also unknown whether the bps1 mobile substance is related to any of these pathways, but its root-to-shoot mobility make it an attractive candidate.
It is also possible that the bps1 mobile compound could instead be an intermediate molecule that normally doesn't accumulate. For example, a biosynthetic pathway might be blocked in bps1 mutants, resulting in build-up of a precursor that happens to be mobile, and happens to have biological activity. For example, in superroot1 mutants, a defect in glucosinolate biosynthesis causes a build-up of precursors that spills over into auxin biosynthesis, resulting in a high-auxin phenotype .
Here, we evaluate the conditions under which bps1 roots produce the mobile compound, and the characteristics of shoots undergoing arrest from this substance. We find that bps1 roots produce and transport the mobile substance in actively growing roots, but that arrest of cell division leads to cessation of signaling to the shoot. Shoot responses include growth cessation, and in particular, arrest of cell division.
The bps1root: shoot growth inhibition requires root growth
The central feature of bps1 mutants is that a growth-arresting mobile compound arises in the root . However, the experimental basis for this assignment required wounding, and it was only tested in very young seedlings. To expand our understanding of the root's role in producing the bps1 signal, we examined how leaf development responded when bps1 root growth and development was blocked after embryogenesis. Post-embryonic root growth and development requires glutathione (GSH, ). Root development can therefore be blocked by either supplying germinating seeds with L-buthionine sulfoximine (BSO), an inhibitor of γ-glutamylcysteine synthetase, or by generating double mutants between bps1 and root meristemless1-1 (rml1-1), which has a defect in the gene encoding γ-glutamylcysteine synthetase and lacks post-embryonic root development [27, 28].
The bps1 shoot phenotype requires post-embryonic root development
Shoot Phenotypes Observed
rml1-1 bps1-2 F2
rml1-1 bps1-2 F2
Analysis of GSH as a candidate for the BPS1-regulated signal
Total bps1with excised root (n)
Percent producing broad leaves with distinct blade and petiole (n)
94% (32) **
Arrested roots provide a transient source of the bps1signal
Arrest of post-embryonic root growth in bps1 caused strikingly different responses in the first leaf pair as compared to leaf three. Both BSO-grown bps1 mutants and rml1 bps1 double mutants initially produced a pair of radialized leaves, yet rescued development was observed in subsequently produced leaves (Figure 1). In addition, the rml1-1 bps1-2 first leaf pair was consistently larger than that of BSO-grown bps1-2 mutants. These results contrast to root excision (carried out at day 4), where the strongest rescue was observed in the first leaf pair , and suggest that the arrested bps1 root might be a transient source of the bps1 mobile compound.
We tested this possibility using the bps1 temperature dependent phenotype . We compared the first leaf pair of bps1 rml1-1 double mutants grown at 16, 22, and 29°C. For bps1 single mutants, leaf development is temperature dependent: severe arrest occurs at low temperatures, and small but flattened leaves are produced at high temperatures. Thus, if the radialized first leaf pair of bps1 rml1-1 double mutants was due to the bps1 mobile signal, then we expected its development to be similarly dependent on growth temperature.
Competence to synthesize and respond to the bps1signal is retained in older seedlings
Although the molecular target of the bps1 root-derived mobile compound is unknown, root-dependent arrest of early shoot development in bps1 seedlings indicates that the target is present at this early stage. However, we do not know if the molecular target is present later in development, nor do we know whether an older root retains the capacity to synthesize the mobile compound. To test this, we followed up on the observation that rml1 root development is rescued by supplying glutathione (GSH) . We reasoned that supplying GSH to an older bps1 rml1 double mutant might restore growth of a bps1-like root. If this root retained the ability to synthesize and deliver the mobile compound, and its molecular target was present in older shoots, then we would expect to observe arrested leaf growth.
The bps1mobile compound: synthesis and delivery require neither the phloem nor endodermis
We next developed double mutants that combined bps1 with altered phloem development (apl), shortroot (shr), and scarecrow (scr) mutants. The apl mutant lacks phloem, shr lacks endodermis, and scr replaces endodermal and cortical cell layers with a single layer of mixed identity [29–33]. We predicted that if the phloem or endodermis were the sole site of synthesis of the bps1 mobile compound, or required for its transmission, then leaf development would be at least partially restored in the double mutants.
shr and scr radial patterning defects do not suppress the bps1 shoot phenotype
Shoot Phenotypes Observed
scr3-9 bps1-2 F3
shr bps1-2 F2
Shoot responses to the bps1mobile root-derived compound
The reversible arrest of shoot development in bps1 mutants correlates with a loss of auxin responses , but the underlying mechanism of arrest is unknown. To broaden our understanding of shoot responses in bps1, we carried out a series of time-course analyses where we analyzed leaf size, shape, the distribution of dividing cells, and stress responses (necrotic lesion formation and appearance of ROS).
While carrying out this analysis of leaf development, we also compared patterns of CYCB1;1::GUS-staining in roots (Figure 5). In the wild type, CYCB1;1::GUS-staining patterns were restricted to the root meristem, as has been described previously , and a similar pattern was observed between days three and seven. By contrast, at all time points, the bps1 root had fewer CYCB1;1::GUS-staining cells.
Physiological studies have implicated long distance signaling as a link between the development and physiology of roots and shoots . However, only a small number of long-distance signaling pathways have been verified molecularly. In Arabidopsis bps1 mutants, the non-cell-autonomous activity of mutant roots suggests that BPS1 might function to limit the synthesis of a root-derived mobile signaling molecule .
Capacity to Synthesize the BPS1 Mobile Compound
A central feature of bps1 mutants is that the root is the source of a biologically active mobile compound, which we refer to as the bps1 signal. Here, we extended our understanding of the conditions under which the mutant root produces this compound. Previously we showed that cutting off the root led to rescue of the first leaf pair . Indeed, we have now found that arresting post-embryonic bps1 root growth also resulted in rescue of leaf development. However, in contrast to root excision, the first leaf pair was only mildly rescued, and strong rescue was delayed until leaf three. These observations indicate that the bps1 root, despite post-embryonic arrest, retained a transient ability to supply the bps1 signal to the shoot.
We used two related approaches to arrest post-embryonic root growth: we caused arrest through the depletion of GSH either genetically (using the rml1-1 mutant) or chemically (using BSO). In both cases, the first leaf pair in GSH-depleted bps1 was larger than that of untreated bps1 mutants, and the first leaf pair of bps1 rml1-1 double mutants were consistently larger than that of BSO-grown bps1. Here, a larger leaf size probably reflects an earlier block to GSH synthesis in the mutant, and therefore an earlier reduction in bps1 signal synthesis.
Similarly, we found that restoring development of bps1 roots (by GSH provision to bps1 rml1-1 seedlings) reinstated arrest of leaf development. The extended capacity to produce and respond to the mobile compound is in line with physiological studies of drought-evoked long distance signaling, which has been documented in diverse plants, and at varying developmental stages .
A possibly less obvious question is why growth-arrested roots (i.e. bps1 rml1-1 double mutants and BSO-grown seedlings) show a decreased ability to arrest shoot growth. One possibility is that bps1 signal synthesis has a direct requirement for GSH. Alternatively, either synthesis or transmission to the shoot requires active root growth and cell division.
The maintenance of shoot arrest in apl bps1 double mutants is consistent with a link to root growth. Although apl mutants have determinate roots , growth ceases later than for rml1-1 or BSO-treated plants, and the apl bps1 analysis was carried out prior to evidence of root cell division arrest. However, if root growth is a requirement for bps1 signal synthesis, then we would need to be able to explain constitutive synthesis of bps1 signal in bps1 mutants, which show primary root arrest soon after germination. One possibility is that synthesis is sustained by lateral roots, which initiate repeatedly. Alternatively, bps1 roots (including the primary) expand radially, and this radial growth might also sustain synthesis of the bps1 signal.
Movement of the bps1 signal from the root to the shoot is likely to use the plant's vascular system. Two vascular tissues are specialized for long-distance movement: the phloem, which transports photosynthate, and also mRNAs and proteins; and the xylem, which primarily transports water and dissolved nutrients. Here, we found that the shoot undergoes arrest in bps1 apl double mutants, which lack phloem . The simplest conclusion is that the bps1 signal moves in the xylem. However, this conclusion is not definitive, because the very small size of bps1 apl double mutants doesn't preclude movement by diffusion.
Shoot responses to the mobile bps1signal
The small leaf size and reduced number of CYCB1;1::GUS expressing cells are a fully penetrant bps1 phenotype. Strikingly, although reduced in number, the pattern of CYCB1;1::GUS-expressing cells mimicked the wild type pattern: leaf primordia showed an even distribution of diving cells, but as the mutant leaves matured, dividing cells were restricted to the base of the leaf. The retention of a normal pattern of dividing cells shows that some aspects of leaf developmental programming persist in bps1 mutants. This result hints that instead of altering development, the bps1 signal might instead disrupt the link between development and cell cycle control.
Another phenotype in bps1 mutants is the formation of necrotic lesions. These were late-appearing and not fully penetrant. Necrotic lesions have been observed in a wide range of Arabidopsis mutants. These include plants with defects in syntaxin genes , and mutants with defects in the cytochrome P450 gene CYP83B1, which results in excess auxin synthesis . Necrosis is typically associated with plant defense responses, and can be a secondary consequence of elevated expression of defense genes, such as observed in the developmental mutant asymmetric leaf 1  and in response to phosphate deficiency [46, 47].
The results presented here support the phenomenon of shoot arrest by a root-derived molecule in bps1 mutants. A key question raised by discovery and characterization of this mutant is whether the bps1 mutation exposes a novel root-to-shoot signaling molecule or a metabolic intermediate with toxic effects on shoot development. The crucial difference between these two concepts is that a novel root-to-shoot signaling molecule would be present in the wild type, while a metabolic intermediate would only accumulate in bps1 mutants. Because the synthesis of the root-derived molecule requires post-embryonic root development and aerial organs appear to arrest growth prior to showing any signs of toxicity (necrosis), we tend to favor the hypothesis that bps1 reveals a novel root-to-shoot signaling pathway. A full resolution of this issue awaits biochemical identification of this mobile molecule. Regardless of the nature of the root-derived compound, it should be pointed out that under either scenario the bps1 mutation has unveiled a molecule with potent biological activity. Despite the impact of root-to-shoot communication on plant productivity, the molecular mechanisms involved are poorly understood. The bps1 mutation could be utilized as a tool to begin to dig into the pathways that both synthesize and respond to root-derived growth modulators.
All seeds were cold-shocked for 2-4 days in darkness at 4°C, and most grown in 24 hour light at the 22°C, unless noted otherwise. Growth media composition is 0.5X MS salts (Caisson labs), 1% sucrose, 0.5g/l MES, pH 5.8, 0.8% phytoblend agar (Caisson Laboratories). Seedlings were grown in Conviron TC30 growth chambers under light and temperature regimes as described.
Mutant alleles used: bps1-2 (Col), bps1-1 (L.er), rml1-1 (Col, received from Z.R. Sung), scr-3 (Col, CS3997), shr (Col, SALK_002744), apl (Col, received from M. Bonke), and CYCB1;1::GUS seeds were received from J.L. Celenza.
The CYCB1;1::GUS transgene was crossed into both bps1-1 and bps1-2, and F3 lines homozygous for the transgene and segregating for bps1 were identified. We plated these lines (and control wild-type transgenic) on normal growth media, and subjected them to a 2-7 day cold shock (4°C). Each day, plates were transferred to a 22°C growth chamber. GUS staining followed previously published protocols .
Conditional Root Arrest
Arrest of roots using BSO was carried out by making our standard GM (above), and supplementing it to 2.5 mM BSO (DL-Buthionine-[S,R]-sulfoximine, Sigma), and bps1-2 rml1-1 double mutants were generated by standard methods. For both BSO and rml1 experiments, plants were grown in short day (8 hours light/16 hours dark) at 22°C. To reinstate root growth of rml1-1, we supplemented the media to 750 μM glutathione (Acros Organics) . To test whether the number of plants producing broad leaves upon root excision in the presence of GSH was statistically different from that observed in the absence of GSH (Table 2), we performed hypothesis testing for proportions using the Z-score method. If GSH were the root-shoot signal, we would predict that the number of plants forming broad leaves under GSH+ conditions would be less than under GSH-conditions (the null hypothesis). The statistical tests indicate that the number of plants producing leaves in the presence of GSH is not less than or equal to the number producing leaves in the absence of GSH. Because the calculated P value is low, we must reject the null hypothesis in support of the alternative hypothesis that the number of plants producing leaves under GSH+ conditions is greater than GSH-conditions. This indicated that the root-to-shoot signal is not GSH.
Stress symptom analyses
Necrotic lesion formation was assessed by a visual inspection of bps1 and wild type seedlings. All organs of the investigated seedlings were examined on alternate days. To visualize patterns of H2O2 in seedlings (wild type and bps1), we used 3,3'-diaminobenzidine (DAB) staining as described [49, 50]. We infiltrated 0.1% (W/V) DAB (Sigma), pH3.8, and allowed staining to progress for 4-6 hours. After staining, samples were cleared in 70% ethanol, and then transferred to 40% w/v glycerol, mounted on glass slides, and examined on Olympus BX50 and Olympus SZX16 microscopes. Visualization of superoxide patterns used nitroblue tetrazolium staining protocols as described [51, 52].
We would like to thank Dong-Keun Lee and Emma Adhikari for useful discussions of the work and for proofreading. This project supported by the National Research Initiative competitive grant no. 2008-35304-04488 (to LES) from the USDA National Institute of Food and Agriculture, by award IOB-0922288 (to LES) from the National Science Foundation, and an award from NSF-supported BioURP award to CM and NIH training grant support to JMVN (NIH training grant number 5 T32 GM007464).
- Last RL, Jones AD, Shachar-Hill Y: Towards the plant metabolome and beyond. Nat Rev Mol Cell Biol. 2007, 8: 167-174. 10.1038/nrm2098.PubMedView ArticleGoogle Scholar
- Sawada Y, Akiyama K, Sakata A, Kuwahara A, Otsuki H, Sakurai T, Saito K, Hirai MY: Widely targeted metabolomics based on large-scale MS/MS data for elucidating metabolite accumulation patterns in plants. Plant Cell Physiol. 2009, 50: 37-47. 10.1093/pcp/pcn183.PubMedPubMed CentralView ArticleGoogle Scholar
- Urano K, Kurihara Y, Seki M, Shinozaki K: 'Omics' analyses of regulatory networks in plant abiotic stress responses. Curr Opin Plant Biol. 2010, 13: 132-138. 10.1016/j.pbi.2009.12.006.PubMedView ArticleGoogle Scholar
- Giavalisco P, Hummel J, Lisec J, Inostroza AC, Catchpole G, Willmitzer L: High-resolution direct infusion-based mass spectrometry in combination with whole 13C metabolome isotope labeling allows unambiguous assignment of chemical sum formulas. Anal Chem. 2008, 80: 9417-9425. 10.1021/ac8014627.PubMedView ArticleGoogle Scholar
- Cui Q, Lewis IA, Hegeman AD, Anderson ME, Li J, Schulte CF, Westler WM, Eghbalnia HR, Sussman MR, Markley JL: Metabolite identification via the Madison Metabolomics Consortium Database. Nat Biotechnol. 2008, 26: 162-164. 10.1038/nbt0208-162.PubMedView ArticleGoogle Scholar
- Meyer RC, Steinfath M, Lisec J, Becher M, Witucka-Wall H, Torjek O, Fiehn O, Eckardt A, Willmitzer L, Selbig J, Altmann T: The metabolic signature related to high plant growth rate in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2007, 104: 4759-4764. 10.1073/pnas.0609709104.PubMedPubMed CentralView ArticleGoogle Scholar
- Lisec J, Meyer RC, Steinfath M, Redestig H, Becher M, Witucka-Wall H, Fiehn O, Torjek O, Selbig J, Altmann T, Willmitzer L: Identification of metabolic and biomass QTL in Arabidopsis thaliana in a parallel analysis of RIL and IL populations. Plant J. 2008, 53: 960-972. 10.1111/j.1365-313X.2007.03383.x.PubMedPubMed CentralView ArticleGoogle Scholar
- Hannah MA, Caldana C, Steinhauser D, Balbo I, Fernie AR, Willmitzer L: Combined transcript and metabolite profiling of Arabidopsis grown under widely variant growth conditions facilitates the identification of novel metabolite-mediated regulation of gene expression. Plant Physiol. 2010, 152: 2120-2129. 10.1104/pp.109.147306.PubMedPubMed CentralView ArticleGoogle Scholar
- Van Norman JM, Frederick RL, Sieburth LE: BYPASS1 negatively regulates a root-derived signal that controls plant architecture. Curr Biol. 2004, 14: 1739-1746. 10.1016/j.cub.2004.09.045.PubMedView ArticleGoogle Scholar
- Van Norman JM, Sieburth LE: Dissecting the biosynthetic pathway for the bypass1 root-derived signal. Plant J. 2007, 49: 619-628. 10.1111/j.1365-313X.2006.02982.x.PubMedView ArticleGoogle Scholar
- Kang YW, Kim RN, Cho HS, Kim WT, Choi D, Pai HS: Silencing of a BYPASS1 homolog results in root-independent pleiotrophic developmental defects in Nicotiana benthamiana. Plant Mol Biol. 2008, 68: 423-437. 10.1007/s11103-008-9384-7.PubMedView ArticleGoogle Scholar
- Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O: MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell. 2005, 8: 443-449. 10.1016/j.devcel.2005.01.009.PubMedView ArticleGoogle Scholar
- Zou J, Zhang S, Zhang W, Li G, Chen Z, Zhai W, Zhao X, Pan X, Xie Q, Zhu L: The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J. 2006, 48: 687-698. 10.1111/j.1365-313X.2006.02916.x.PubMedView ArticleGoogle Scholar
- Sorefan K, Booker J, Haurogne K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C, Leyser O: MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev. 2003, 17: 1469-1474. 10.1101/gad.256603.PubMedPubMed CentralView ArticleGoogle Scholar
- Morris SE, Turnbull CG, Murfet IC, Beveridge CA: Mutational analysis of branching in pea. Evidence that Rms1 and Rms5 regulate the same novel signal. Plant Physiol. 2001, 126: 1205-1213. 10.1104/pp.126.3.1205.PubMedPubMed CentralView ArticleGoogle Scholar
- Stirnberg P, van De Sande K, Leyser HM: MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development. 2002, 129: 1131-1141.PubMedGoogle Scholar
- Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O: The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol. 2006, 16: 553-563. 10.1016/j.cub.2006.01.058.PubMedView ArticleGoogle Scholar
- Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF: Strigolactone inhibition of shoot branching. Nature. 2008, 455: 189-194. 10.1038/nature07271.PubMedView ArticleGoogle Scholar
- Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S: Inhibition of shoot branching by new terpenoid plant hormones. Nature. 2008, 455: 195-200. 10.1038/nature07272.PubMedView ArticleGoogle Scholar
- Davies W, Zhang J: Root Signals and the Regulation of Growht and Development of Plants in Drying Soil. Annual Rev Plant Physiol Plant mol Biol. 1991, 42: 55-76. 10.1146/annurev.pp.42.060191.000415.View ArticleGoogle Scholar
- Mulholland BJ, Black CR, Taylor IB, Roberts JA, Lenton JR: Effect of soil compaction on barley (Hordeum vulgare L.) growth 1. Possible role for ABA as a root-sourced chemical signal. Journal of Experimental Botany. 1996, 47: 539-549. 10.1093/jxb/47.4.539.View ArticleGoogle Scholar
- Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK: A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol. 2005, 15: 2038-2043. 10.1016/j.cub.2005.10.016.PubMedView ArticleGoogle Scholar
- Bari R, Datt Pant B, Stitt M, Scheible WR: PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 2006, 141: 988-999. 10.1104/pp.106.079707.PubMedPubMed CentralView ArticleGoogle Scholar
- Forde BG: The role of long-distance signalling in plant responses to nitrate and other nutrients. J Exp Bot. 2002, 53: 39-43. 10.1093/jexbot/53.366.39.PubMedView ArticleGoogle Scholar
- Tong H, Leasure CD, Hou X, Yuen G, Briggs W, He ZH: Role of root UV-B sensing in Arabidopsis early seedling development. Proc Natl Acad Sci USA. 2008, 105: 21039-21044. 10.1073/pnas.0809942106.PubMedPubMed CentralView ArticleGoogle Scholar
- Mikkelsen MD, Naur P, Halkier BA: Arabidopsis mutants in the C-S lyase of glucosinolate biosynthesis establish a critical role for indole-3-acetaldoxime in auxin homeostasis. Plant J. 2004, 37: 770-777. 10.1111/j.1365-313X.2004.02002.x.PubMedView ArticleGoogle Scholar
- Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, Van Montagu M, Inze D, May MJ, Sung ZR: The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell. 2000, 12: 97-110. 10.1105/tpc.12.1.97.PubMedPubMed CentralView ArticleGoogle Scholar
- Cheng JC, Seeley KA, Sung ZR: RML1 and RML2, Arabidopsis genes required for cell proliferation at the root tip. Plant Physiol. 1995, 107: 365-376. 10.1104/pp.107.2.365.PubMedPubMed CentralView ArticleGoogle Scholar
- Bonke M, Thitamadee S, Mahonen AP, Hauser MT, Helariutta Y: APL regulates vascular tissue identity in Arabidopsis. Nature. 2003, 426: 181-186. 10.1038/nature02100.PubMedView ArticleGoogle Scholar
- Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT, Aeschbacher RA: Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development. 1993, 121: 53-62.Google Scholar
- Scheres B, DiLaurenzio L, Willemsen V, Hauser MT, Janmaat K, Weisbeek P, Benfey PN: Mutations affecting the radial organization of the Arabidopsis root display specific defects throughout the radial axis. Development. 1995, 121: 53-62.Google Scholar
- Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN: The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell. 1996, 86: 423-433. 10.1016/S0092-8674(00)80115-4.PubMedView ArticleGoogle Scholar
- Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN: The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell. 2000, 101: 555-567. 10.1016/S0092-8674(00)80865-X.PubMedView ArticleGoogle Scholar
- Colon-Carmona A, You R, Haimovitch-Gal T, Doerner P: Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J. 1999, 20: 503-508. 10.1046/j.1365-313x.1999.00620.x.PubMedView ArticleGoogle Scholar
- Kang J, Dengler N: Cell cycling frequency and expression of the homeobox gene ATHB-8 during leaf vein development in Arabidopsis. Planta. 2002, 216: 212-219. 10.1007/s00425-002-0847-9.PubMedView ArticleGoogle Scholar
- Beeckman T, Burssens S, Inze D: The peri-cell-cycle in Arabidopsis. J Exp Bot. 2001, 52: 403-411.PubMedView ArticleGoogle Scholar
- Dong X, Mindrinos M, Davis KR, Ausubel FM: Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell. 1991, 3: 61-72. 10.1105/tpc.3.1.61.PubMedPubMed CentralView ArticleGoogle Scholar
- Heath MC: Hypersensitive response-related death. Plant Mol Biol. 2000, 44: 321-334. 10.1023/A:1026592509060.PubMedView ArticleGoogle Scholar
- Kovtun Y, Chiu WL, Tena G, Sheen J: Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA. 2000, 97: 2940-2945. 10.1073/pnas.97.6.2940.PubMedPubMed CentralView ArticleGoogle Scholar
- Manzano D, Fernandez-Busquets X, Schaller H, Gonzalez V, Boronat A, Arro M, Ferrer A: The metabolic imbalance underlying lesion formation in Arabidopsis thaliana overexpressing farnesyl diphosphate synthase (isoform 1S) leads to oxidative stress and is triggered by the developmental decline of endogenous HMGR activity. Planta. 2004, 219: 982-992. 10.1007/s00425-004-1301-y.PubMedView ArticleGoogle Scholar
- Ogawa K, Kanematsu S, Asada K: Generation of superoxide anion and localization of CuZn-superoxide dismutase in the vascular tissue of spinach hypocotyls: their association with lignification. Plant Cell Physiol. 1997, 38: 1118-1126.PubMedView ArticleGoogle Scholar
- Whetten RW, MacKay JJ, Sederoff RR: Recent Advances in Understanding Lignin Biosynthesis. Annu Rev Plant Physiol Plant Mol Biol. 1998, 49: 585-609. 10.1146/annurev.arplant.49.1.585.PubMedView ArticleGoogle Scholar
- Zhang Z, Lenk A, Andersson MX, Gjetting T, Pedersen C, Nielsen ME, Newman MA, Hou BH, Somerville SC, Thordal-Christensen H: A lesion-mimic syntaxin double mutant in Arabidopsis reveals novel complexity of pathogen defense signaling. Mol Plant. 2008, 1: 510-527. 10.1093/mp/ssn011.PubMedView ArticleGoogle Scholar
- Smolen G, Bender J: Arabidopsis cytochrome P450 cyp83B1 mutations activate the tryptophan biosynthetic pathway. Genetics. 2002, 160: 323-332.PubMedPubMed CentralGoogle Scholar
- Nurmberg PL, Knox KA, Yun BW, Morris PC, Shafiei R, Hudson A, Loake GJ: The developmental selector AS1 is an evolutionarily conserved regulator of the plant immune response. Proc Natl Acad Sci USA. 2007, 104: 18795-18800. 10.1073/pnas.0705586104.PubMedPubMed CentralView ArticleGoogle Scholar
- Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, Deng XW: Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol. 2003, 132: 1260-1271. 10.1104/pp.103.021022.PubMedPubMed CentralView ArticleGoogle Scholar
- Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ: Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol. 2003, 132: 578-596. 10.1104/pp.103.020941.PubMedPubMed CentralView ArticleGoogle Scholar
- Deyholos MK, Cavaness GF, Hall B, King E, Punwani J, Van Norman J, Sieburth LE: VARICOSE, a WD-domain protein, is required for leaf blade development. Development. 2003, 130: 6577-6588. 10.1242/dev.00909.PubMedView ArticleGoogle Scholar
- Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB: Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant Journal. 1997, 11: 1187-1194. 10.1046/j.1365-313X.1997.11061187.x.View ArticleGoogle Scholar
- Ahn IP, Kim S, Lee YH, Suh SC: Vitamin B1-induced priming is dependent on hydrogen peroxide and the NPR1 gene in Arabidopsis. Plant Physiol. 2007, 143: 838-848. 10.1104/pp.106.092627.PubMedPubMed CentralView ArticleGoogle Scholar
- Hoffmann A, Hammes E, Plieth C, Desel C, Sattelmacher B, Hansen U-P: Effect of CO2 supply on formation of reactive oxygen species in Arabidopsis thaliana. Protoplasma. 2005, 227: 3-9. 10.1007/s00709-005-0133-3.PubMedView ArticleGoogle Scholar
- Giraud E, Ho LH, Clifton R, Carroll A, Estavillo G, Tan YF, Howell KA, Ivanova A, Pogson BJ, Millar AH, Whelan J: The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol. 2008, 147: 595-610. 10.1104/pp.107.115121.PubMedPubMed CentralView ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.