Plant Physiology Preview. Published on June 15, 2016, as ... · 12 Department of Biology,...

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Running title: Stress and juvenility in maize 1 2 3 Corresponding author: Erin Irish, Department of Biology, The University of Iowa, 319-335-4 2582, [email protected] 5 6

Plant Physiology Preview. Published on June 15, 2016, as DOI:10.1104/pp.15.01707

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7 8 The juvenile phase of maize sees upregulation of stress-response genes and is extended by 9 exogenous JA 10 Benjamin Beydler, Krista Osadchuk, Chi-Lien Cheng, J. Robert Manak, Erin E. Irish 11 Department of Biology, University of Iowa, Iowa City, Iowa USA 12 13 The juvenile phase of maize is correlated with elevated expression of stress-related genes 14 15



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Financial Support: This work was supported by NSF 0820562. BB was also supported by Avis 16 Cone Summer Fellowships. 17 Corresponding author: Erin Irish, [email protected] 18 19



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Abstract 20 21 As maize (Zea mays) plants undergo vegetative phase change from juvenile to adult, they both 22 exhibit heteroblasty, an abrupt change in patterns of leaf morphogenesis, and gain the ability to 23 produce flowers. Both processes are under the control of microRNA 156, whose levels decline at 24 the end of the juvenile phase. Gain of ability to flower is conferred by expression of miR156 25 targets that encode Squamosa Promoter-Binding (SBP) transcription factors, which when 26 derepressed in the adult phase induce the expression of MADS-box transcription factors that 27 promote maturation and flowering. How gene expression, including targets of those miRNAs, 28 differs between the two phases remains an open question. Here, we compare transcript levels in 29 primordia that will develop into juvenile or adult leaves to identify genes that define these two 30 developmental states and may influence vegetative phase change. In comparisons among 31 successive leaves at the same developmental stage of plastochron 6, three-fourths of 32 approximately 1,100 differentially expressed genes were more highly expressed in primordia of 33 juvenile leaves. This juvenile set was enriched in photosynthetic genes, particularly those 34 associated with cyclic electron flow at photosystem I, and in genes involved in oxidative stress 35 and retrograde redox signaling. Pathogen- and herbivory-responsive pathways including salicylic 36 acid and jasmonic acid were also up-regulated in juvenile primordia and indeed, exogenous 37 application of jasmonic acid both delayed the appearance of adult traits and the decline in 38 expression of miR156-encoding loci in maize seedlings. We hypothesize that the stresses 39 associated with germination promote juvenile patterns of differentiation in maize. 40 41



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Introduction 42 The juvenile phase of vegetative shoot development in angiosperms, defined by lack of 43

competence to flower, dedicates seedlings of annual species to successful establishment (Poethig 44 2013). As development proceeds, plants gain the ability to flower, marking them as adult. Phase 45 in many species of both annuals and woody plants can also be distinguished by heteroblastic 46 variation between juvenile and adult leaves. Phase-associated heteroblasty in maize is a 47 developmentally rich phenomenon, spanning a variety of traits (Dudley and Poethig 1993). For 48 example, the shorter, rounder juvenile leaves lack trichomes but have a waxy epidermis whose 49 cell walls are devoid of lignin and wavy in peridermal view. Adult leaves, in contrast, have a 50 hairy epidermis lacking wax, and the walls of epidermal cells are reinforced with lignin and 51 crenulated. They also possess the bulliform cells that curl the leaves in drought conditions. Such a 52 variety in phase-specific traits supports the view that phase change is not simply the gain of 53 ability to flower but rather is a systemic maturation. 54

Vegetative phase change is under the control of a circuit of miRNA-regulated genes. The 55 juvenile phase is defined by the duration of microRNA 156 expression, miR156 being necessary 56 and sufficient for juvenility in Arabidopsis (Wu et al 2009) and other plants (Wang et al 2011). In 57 Arabidopsis, miR156 expression is established early in embryogenesis (Nodine et al 2010). Its 58 levels are high in germinating seedlings but then declines to end the juvenile phase (Yang et al 59 2011). The Corngrass mutation of maize causes prolonged expression of two of its 12 miR156 60 loci, thereby extending the juvenile phase (Chuck et al 2007). The relief of miR156 repression of 61 target transcripts of SQUAMOSA PROMOTER-BINDING (SBP) transcription factors (Preston 62 and Hileman 2013) confers floral competence by activating the transcription of genes encoding 63 several MADS transcription factors that promote flowering (Yamaguchi et al 2009, Wang et al 64 2009a). SBPs also regulate flowering through the expression of microRNA 172, which targets 65 the transcripts of AP2 transcription factors, some of which inhibit flowering (Zhu and Helliwell 66 2011). Another miR172 target in maize, GLOSSY15, is involved in heteroblasty, conferring 67 juvenile leaf epidermis traits (Moose and Sisco 1996). Although regulation of miR172 and SBP 68 as well as many of the interactions downstream are known (Huijser and Schmid 2011), what 69 causes the levels of miR156 to be high at germination and later decline remain open questions. 70

It has been demonstrated in several species that the decline in miR156 levels in the shoot 71 is mediated by a signal from juvenile leaves and not other parts of the plant (Yang et al 2013). 72 Experimental manipulation of sugar levels supported the conclusion that sucrose is that signal 73 (Yu et al 2013, Yang et al 2013). Aside from a requirement for protein synthesis and the 74 involvement of both transcriptional and post-transcriptional repression (Yu et al 2013), the 75



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molecular mechanism by which sugars repress miR156 is unknown. The hormone gibberellic 76 acid is also capable of advancing the timing of vegetative phase change in maize (Evans and 77 Poethig 1995) although whether it does so by reducing miR156 levels has not yet been 78 determined: miR156 levels are unaffected by a GA deficiency in rice that delays phase change 79 (Tanaka 2012). Rather, given the binding between DELLA proteins and SBPs, GA likely relieves 80 DELLA inhibition of SBP protein activity (Yu et al 2012) which in turn activates the 81 transcription of the SBP-responsive MADS factors genes (Mutasa-Göttgens and Hedden 2009). 82

In order to identify candidate components of the networks both underlying the suite of 83 phase-specific traits and effecting vegetative phase change in maize, we conducted a systematic 84 comparison of gene expression in juvenile vs. adult leaves. Leaves were chosen for this study 85 because although meristems initiate the leaf, the specification of the leaf’s phase identity occurs 86 after the primordium is well established (Irish and Karlen 1996, Orkwiszewski and Poethig 87 2000), and because leaves have been shown to provide signals that influence miR156 levels 88 (Yang et al 2013). We examined leaves at plastochron 6, a stage long before any patterns of 89 differentiation appear (Sylvester et al 1990), taking advantage of the relatively large shoot 90 meristem and the primordia it produces. Gene expression microarrays were employed to compare 91 transcript levels among each of the first twelve leaves, thus spanning the set made from early 92 post-germination at the beginning of the juvenile phase to well into the adult phase. The 93 transcriptomes of juvenile leaf primordia were found to differ from those of adult leaf primordia 94 largely in their higher expression of many photosynthetic and stress-responsive genes, confirming 95 our previous results examining a smaller set of probes and leaves (Strable et al. 2008). These 96 genes were tightly co-expressed in a small number of hierarchical clusters, and many shared 97 sequence motifs in upstream regions, pointing to common regulation. Treatment with the stress-98 associated hormone, jasmonic acid, prolonged the juvenile phase and delayed the decline in 99 miR156 levels, whereas reduced-JA mutants showed early phase change. Our results are 100 consistent with the hypothesis that stress responses play a part in promoting the juvenile state in 101 this annual species. 102 103



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Results 104 Each successive juvenile leaf is less different; adult leaves are the same 105

When fully expanded, juvenile and adult leaves of maize differ by a number of 106 morphological traits, but at plastochron 6 all maize leaves are identical in appearance: tiny and 107 pale yellow, with only the first veins apparent. Using microarray analysis we found that at this 108 early stage there were nonetheless large differences in patterns of gene expression. In pairwise 109 comparisons of the first 12 leaf primordia, 16,772 transcripts (42.2% of the filtered gene set) 110 showed at least a two-fold difference in expression between any two of the 12 samples. Genome-111 wide similarity (Pearson r2) of expression of these so-called dynamic transcripts ranged from 0.53 112 (leaves 1 and 10) to 0.98 (leaves 10 and 11, Figure 1A). The first-formed, juvenile leaves were 113 most distinct, with steadily decreasing differences in gene expression profiles, leaves 7-12 being 114 most similar. Pairwise comparisons excluding leaves 1 or 2 gave r2 values of 0.80 or greater; 115 comparisons among leaves 6 through 11 had values of 0.95 or greater. Likewise, hierarchical 116 clustering separated primordia of leaves 1 and 2 as the most distinct, with leaves 3 and 4 and leaf 117 5 also clustering separately from the later-formed leaves (Figure 1B). These divisions are 118 consistent with the observed morphology in the genetic background used, in which leaf 4 is the 119 last with wholly juvenile identity (waxy, hairless, no lignin) and leaf 6 the first with majority 120 adult identity (hairs over most of leaf surface, lignin present), and with previous work suggesting 121 that the first two maize leaves are distinct from other juvenile leaves (Bongard-Pierce et al. 1998). 122

Examination of expression patterns among dynamically expressed genes led to our 123 categorization as phase specific any gene that showed either at least a two-fold difference in 124 expression between most juvenile and most adult samples, or at least a five-fold difference 125 between the first two leaves and adult leaves. In comparisons of representative juvenile and adult 126 leaf primordia, leaves 1-3 and 9-11 respectively (which also were sets of the least and most 127 similar samples), we found that 1,107 transcripts (2.8% of the filtered gene set) showed 128 significantly higher expression in one of the two phases (Supplementary table 1). Some 921 129 transcripts were at least two fold more highly expressed in the juvenile leaves in all nine 130 comparisons and/or were at least 5 fold more highly expressed in the 6 comparisons involving 131 leaves one and two. Some 243 transcripts were more highly expressed in the adult leaves. Gene 132 ontology analysis of the juvenile and adult sets of phase-specific genes identified photosynthesis 133 as by far the most significantly enriched juvenile term, followed by involvement in oxidation 134 reduction (redox) reactions and immune processes (Table 1). The adult set was enriched in 135



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transcriptional regulators, also in agreement with earlier work in which a smaller set of genes was 136 examined (Strable et al 2008). 137

To confirm our criteria for identifying phase-specific genes, we subjected the dynamic 138 transcripts to hierarchical clustering. Both juvenile and adult gene sets were positioned within 139 distinct clusters (Figure 1C). Some 86% of the adult-specific genes were located within a single 140 4,196 transcript cluster and 94% of juvenile-specific genes were located within a single 3,385 141 transcript cluster (Figure 1C). The latter cluster, 25.6% of which had met our criteria as juvenile-142 specific transcripts, cleanly subdivided into approximate halves, with an early juvenile cluster 143 (1,760 transcripts) characterized by high expression limited to the first two leaf primordia and a 144 so-called full-juvenile cluster (1,625 transcripts) where high expression extended into the third 145 and fourth leaf primordia (Figure 2). GO analysis indicated that these two juvenile subclusters 146 were enriched in different functions; redox reactions and stress responses were especially high in 147 the first two leaves while photosynthetic and chlorophyll biosynthesis genes were highly 148 expressed throughout the juvenile phase (Table 1). 149 Transcriptional regulators show phase specificity 150

Maize has 12 miR156 loci, miR156a-l. Whereas the expression patterns of individual loci 151 varied substantially, their overall expression tended to decrease sharply during the juvenile phase, 152 with highest levels in leaf one, lower but equivalent levels in leaves 2 and 3, a step down in 153 leaves 4 and 5, and a constant lower level in subsequent leaves. The most highly expressed loci 154 were miR156g and miR156f, which were tightly co-regulated (r2 > 0.97) and were located in the 155 full juvenile cluster, as were miR156i and miR156l (Figure 2). miR156h and miR156e were 156 located in the early juvenile cluster. miR156j and the two overexpressed in Cg1 mutants, 157 miR156b and miR156c (Chuck et al, 2007), were minimally expressed in plastochron 6 leaf 158 primordia (not shown). miR172 expression was appreciable from only one locus, miR172c 159 (Figure 3), which increased 18-fold between leaves 1 and 5 and continued to increase in 160 expression in successive leaves. The other four miR172 loci, including miR172e, whose loss of 161 function is the tasselseed4 mutation, were minimally expressed (not shown) in plastochron 6 162 primordia. 163

During vegetative phase change, the decline of miR156 expression results in upregulation 164 of SBP transcription factors in primordia of leaves destined to become adult. Of the 32 SBPs in 165 maize, 19 were differentially expressed at plastochron 6, including six that lack miR156 target 166 sites. Transcript levels are, of course, only reflective of miR156 regulation by transcript cleavage; 167 inhibition of translation is also almost assured, as has been observed in Arabidopsis miR156 168 regulation (Gandikota et al 2007). Transcription factors were overrepresented among the 169



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relatively few classes of transcripts that were strongly adult-upregulated (Table 1). Mapman 170 analysis found the adult-upregulated SBP, B3, and MADS families to be the most phase biased 171 (Table 2). Genes encoding several SBP (8,9,13,25,29) and MADS (1,9,56,72,76) factors were 172 coexpressed and within the same expression subcluster as miR172c using Pearson hierarchical 173 clustering (Figure 3). This is in agreement with the known SBP stimulation of MADS factors that 174 promote maturation and flowering (Yamaguchi et al 2009, Wang et al 2009a) and of miR172 175 (Zhu and Helliwell 2011). SBP13 and SBP29 showed the greatest increases in transcript level. 176 MADS1, MADS56, and MADS76 are putative orthologs of AtSOC1, which represses the 177 expression of miR156 and juvenile AP2 factors by binding to their promoter sequences (Immink 178 et al 2012). MADS72 (tunicate1) is a putative ortholog of AtSHORT VEGETATIVE PHASE, 179 which stimulates transcription of miR172a by binding its promoter (Cho et al 2012a). 180 Transcription factors overrepresented in the juvenile phase included the CONSTANS-like zinc 181 finger, GATA zinc finger, AP2, and GRAS families (Table 2). 182

Promoter motif analysis of genes coexpressed in the hierarchical clustering with the two 183 miRNAs showing strongest phase-biased expression, miR156f/g/i and miR172c, was conducted 184 on the 400 bp upstream regions using SCOPE (Chakravarty et al 2007) and DREME (Bailey and 185 Elkan 1994). These analyses identified motifs associated chiefly with light-responsive 186 transcription factors in juvenile-upregulated genes (Figure 4A) and MADS proteins in adult 187 (Figure 4B). The MADS binding-like motif of the proximal region of miR156-coexpressed genes 188 (“miR156 proximal”), AWADAAA, is most similar to the binding recognition sequence of 189 AtSOC1. The miR172 proximal regions were enriched in a similar motif, AWAWAWA, which is 190 also predicted to be a recognition site for multiple MADS factors. A large proportion (43.5%) of 191 miR156 proximal regions contained the motif ACGTRS, often as a staggered palindrome. This 192 sequence is similar to the canonical G-box motif CACGTG recognized by phytochrome-193 interacting factors (PIFs) (Martínez-García et al 2000). Regulation of the juvenile photosynthetic 194 cluster by light is also suggested by the motif CACGSSC, similar to the FAR-RED 195 ELONGATED HYPOCOTYL3 (FHY3) binding site CACGCGC (Figure 4A); FHY3 integrates 196 phytochrome A signaling with the circadian clock (Ouyang et al 2011). 197

198 Phloem-mobile stress signals delay vegetative phase change 199

The enrichment of the early juvenile phase in stress signaling transcripts (Table 1, Figure 200 5) prompted us to hypothesize that the potential stresses that accompany seedling establishment 201 in light might be among the factors that promote juvenility. The abundance of transcripts 202 encoding enzymes that catalyze the synthesis or modification of salicylic acid (SA), which is 203



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produced in response to biotrophic pathogens, and jasmonic acid (JA), which is produced in 204 response to necrotrophic pathogens and insects and to abiotic stresses such as drought, suggested 205 high levels of these phytohormones in juvenile primordia. Genes encoding methyltransferases 206 that synthesize methyl salicylate (MeSA) and methyl jasmonate (MeJA) were strongly expressed; 207 MeSA has been demonstrated to be a phloem-mobile form of SA (Park et al 2007). Three JA-208 induced proteins (JIPs) were among the most highly expressed juvenile transcripts (Supplemental 209 Table 1). The expression of a gene encoding a 23kD JIP, which has been shown to localize to 210 phloem (Hause et al 1996), strongly correlated with that of several miR156 loci (r2: 0.93 with 211 miR156f). Because of the upregulation of JA-associated genes in our data and reduced miR156 212 levels in JA-deficient tasselseed1 mutants (Hultquist and Dorweiler 2008, Acosta et al 2009), JA 213 emerged as a likely signaling candidate. Application of JA to the apical whorl of seedlings was 214 indeed sufficient to delay the appearance of adult traits in transition leaves, which, in accordance 215 with the basipetal pattern of differentiation in maize leaves, display juvenile traits at the tip and 216 adult traits at the base (Fig. 6). Epidermal trichomes, staining patterns signifying the presence of 217 lignin in cell walls (O’Brien et al 1964), and bulliform cells were all displaced basipetally in a 218 JA-dosage-dependent manner. In contrast, those adult traits appeared precociously in ts1 mutants. 219 Treatment with 30% H2O2 similarly delayed vegetative phase change while 100mM SA had a 220 modest but non-significant juvenilizing effect (Supplemental Fig. 1). 221

To determine whether JA-extended juvenility was associated with a prolonged period of 222 high expression at miR156 loci, plastochron 6 primordia of leaf 5 from seedlings that had 223 previously been treated with a single application of 15 mM JA were subjected to microarray 224 analysis. Overall, JA-treated leaf 5 was much more similar to untreated leaves 3 (r2 of 0.81) or 4 225 (r2 of 0.79) than to untreated leaf 5 (r2 of 0.69), mirroring the effect on leaf size (JA-treated leaf 5 226 was only as long as untreated leaf 3), and hierarchical clustering using phase-specific genes 227 placed treated leaf 5 with leaves 3 and 4 (Fig. 6G). Significantly, the “full juvenile” miR156’s f, 228 g, and i were each 2-fold higher in expression, while miR172c was more than 12-fold lower in 229 JA-treated plants (Supplemental Table 2), compared to untreated leaf 5. Transcripts of SBP’s and 230 other transcription factors were also broadly lower. Unsurprisingly, a JIP-encoding gene was 231 among the most highly expressed in treated leaves with a greater than 170-fold increase compared 232 to untreated leaf 5, exceeded only by expression of a lipoxygenase and an O-methyltransferase 233 gene. 234 235 Juvenile expression of diverse stress-associated genes 236



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In addition to genes involved in stress hormone production, other stress-related genes showed 237 highly elevated expression, in two distinct patterns. Genes encoding six of the maize SNF1-238 Related Kinases (SnRKs), which are central effectors of energetic stress responses, were tightly 239 coexpressed in leaves one and two (Figure 7a). Several glutathione s-transferase genes (GSTs), 240 which conjugate glutathione to other proteins to maintain redox homeostasis, were similarly 241 upregulated in the early juvenile leaf primordia (Figure 7). In contrast, several m- and f-type 242 thioredoxin genes were highly expressed in all juvenile leaf primordia and coexpressed with 243 miR156 (Figure 7b). 244 245



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Discussion 246 The data presented here support the hypothesis that stress is among the factors that 247

promote and maintain the juvenile phase in maize seedlings, and that, once stress is relieved, the 248 plant converts to adult patterns of differentiation. Although the first four or five leaves of maize, 249 which are those with juvenile traits, are initiated during embryogenesis, even the first leaf shows 250 minimal differentiation in the dry seed (Liu et al 2013), and thus juvenility might be expected to 251 be imposed during the process of germination. The most obvious stressor specific to juvenile 252 leaves is photo-oxidative stress – upon emergence from the soil, seedling leaves must 253 immediately commence management of absorbed light energy. Whereas throughout the growing 254 season each new leaf expanding into light is likely also to experience such stress, in the case of 255 the seedling the entire shoot undergoes de-etiolation. Chloroplasts are a major source of ROS in 256 plant cells and chloroplast-generated ROS are a main pathway of retrograde regulation (Estavillo 257 et al 2013, Trotta et al 2014). ROS peroxidation of membrane lipids forms phytoprostanes, which 258 induce some of the same stress-responsive networks as JA (Stotz et al 2013). Stress responses 259 acting to prolong the juvenile phase is not difficult to reconcile with demonstrations that miR156 260 expression is sugar-repressible (Yu et al 2013, Yang et al 2013). Many abiotic stresses converge 261 on metabolic signaling pathways (Radomiljac et al 2013, Tomé et al 2014) and metabolism is 262 linked generally to oxidative stress through redox regulation of Calvin cycle enzymes (Michelet 263 et al 2013). Several conserved gene families involved in production of possible cell-autonomous 264 juvenilizing factors that may regulate development downstream of abiotic stress pathways 265 emerged from this study. 266

SNF1-Related Kinases (SnRKs), the plant homologs of yeast SNF1 and mammalian 267 AMPK, are central effectors of energetic stress responses. Plant SnRKs have widely diversified 268 beyond the ancestral SnRK1 subfamily, with distinct plant-specific SnRK2 and SnRK3 269 subfamilies that likely integrate metabolism with other stress responses (Halford and Hey, 2009). 270 Our data identify SnRKs as present in both the adult and juvenile clusters, with a tightly 271 coexpressed early juvenile group of six SnRK3s as especially prominent. No phase change 272 phenotype has yet been described for SnRK3 mutants, although SnRK1 regulation clearly affects 273 developmental timing – this has been demonstrated by multiple studies in which overexpression 274 delayed flowering and vegetative phase change (Baena-González et al 2007, Tsai and Gazzarrini 275 2012,Williams et al 2014) – and Snrk 3s have been demonstrated to interact with Snrk1 in the 276 regulation of sugar responses (Yan et al 2014). Further, interaction has been shown between 277 SnRKs and the B3 transcription factor FUSCA3, which binds to the promoters of miR156 loci 278 (Gazzarrini et al 2004). 279



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Several GSTs, which conjugate glutathione to other proteins to maintain redox 280 homeostasis, were also highly juvenile-upregulated. Two are putative homologs of AtGSTU17, 281 which substantially increases leaf number when mutated and decreases it when overexpressed 282 (Chen et al 2012). Interestingly, several GSTs were identified as down-regulated in an miR156-283 overexpressing line of switchgrass (Fu et al 2012). The juvenile upregulation in maize, taken 284 together with the GST-overexpression phenotypes in Arabidopsis and switchgrass, suggest that 285 miR156 shares stress-responsive regulatory pathways with a subset of GSTs, and also that some 286 GST activity likely promotes vegetative phase change. GSTs could conceivably encourage 287 maturation by ameliorating developmentally inhibitory stress downstream of oxidative products 288 like phytoprostanes (Stotz et al 2013) or through broader interactions between antioxidants and 289 immunity (Han et al 2013). 290 The extensively diversified plant thioredoxins link redox homeostasis and development 291 through the activity of chloroplast proteins. Several m- and f-type thioredoxins were highly 292 coexpressed with miR156 in juvenile primordia. m-type thioredoxins have been shown to inhibit 293 CEF (Courteille et al 2013) and to be required for plasmodesmatal flow and SAM maintenance 294 (Benitez-Alfonso et al 2009). The tetrapyrrole pathway ultimately produces chlorophyll, and 295 synthetic intermediates of heme are major regulators of retrograde signaling (Estavillo et al 2013, 296 Terry and Smith 2013). Thioredoxin control of retrograde signaling through the tetrapyrrole 297 pathway is well established (reviewed in Serrato et al 2013) and is also suggested in our data by 298 coexpression or thioredoxins and tetrapyrrole synthesis enzymes (Figure 6). 299

It has been shown that JA induces DELLA proteins, which function to target the JA ZIM-300 domain proteins that repress JA-inducible gene expression (Wild et al 2012); thus JA may 301 promote DELLA repression of SBP activity, thereby preventing flowering. JA and MeJA 302 treatment has been shown to decrease the expression of SBP genes both with and without a 303 miR156 binding site in V. vinifera (Hou et al 2013). JA and GA signaling through DELLAs is 304 known to be antagonistic (Yang et al 2012), with JA-deficiency increasing GA sensitivity and 305 vice versa. DELLAs also closely regulate oxidative stress responses by promoting the expression 306 of detoxifying elements including superoxide dismutases and GSTs (Achard et al 2008). 307

miRNAs 156 and 172 regulate phase change in woody species as well as Arabidopsis and 308 maize (Wang et al, 2011). If stress is a common inducer of juvenility, acting by promoting high 309 levels of miR156 in trees, other mechanisms would be expected to be involved in sustaining the 310 juvenile phase, which can persist for decades. Stress as an inducer of juvenility in maize provides 311 an appealing explanation for the phenomenon of rejuvenation by shoot apex culture in maize 312



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(Irish and Karlen, 1998); indeed, stress-associated genes were among those identified as most 313 highly up-regulated in culture-reset leaves (Strable et al., 2008). 314

315 Materials and Methods 316 Plant material and growth conditions 317 B73 and Mo17 (seeds kindly provided by P. Schnable) were crossed to generate hybrid seeds, 318 which were planted and grown in a temperature-controlled greenhouse and illuminated for 14 319 hours daily under 1kW metal halide and sodium lights (www.osram.com). Seeds segregating for 320 tasselseed1 seeds were a gift from Josh Strable. Plants were grown in Compost Plus growing mix 321 (www.beautifullandproducts.com). Leaf primordia at the developmental stage of plastochron 6, 322 measured as a length of 8(+/-2) mm, were selected for analysis, based on unpublished RT-PCR 323 comparison of expression of genes identified in a previous study of gene expression during 324 vegetative phase change in maize (Strable et al 2008). In this genetic background, leaves 1-4 325 displayed only juvenile traits, leaves 5-7 were transition leaves with successive leaves displaying 326 increasing amounts of adult tissue, and leaf 8 and above were entirely adult in morphology. 327 RNA isolation and cDNA synthesis 328 Leaf primordia were isolated by dissection of shoot tips and flash-frozen in liquid nitrogen. Total 329 RNA was extracted by Trizol (www.lifetechnologies.com) and purified on RNeasy columns 330 (www.qiagen.com) using the manufacturer’s protocols. Double-stranded cDNA was synthesized 331 using Superscript III reverse transcriptase with an oligo-dT primer according to the NimbleGen 332 gene expression protocol booklet. 333 Microarray design and data normalization 334 A custom microarray designed by us in consultation with Roche NimbleGen (NimbleGen, 335 Madison, WI) representing the primary transcripts of genes in the maizeGDB.org RefGen_v2 336 filtered gene set (39,656 genes) and 171 known maize microRNA precursor transcripts from 337 mirbase.org (Supplemental Table 1) was used in these experiments. Arrays contained 120,000 338 60-mer probes, with three probes corresponding to each gene or miRNA transcript, which were in 339 turn represented in triplicate. Array data were scaled in Array Star 4 (www.dnastar.com) using 340 Robust Multi-array Average (RMA) analysis with quantile normalization. Twelve arrays (three 341 biological replicates with four technical replicates each) were initially hybridized. R2 values 342



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among biological replicates were considered sufficiently high (≥0.98) that all subsequent samples 343 were assayed by three technical replicates. 344 To identify differentially expressed genes, pairwise Student’s t-tests with Benjamini-Hochberg 345 multiple testing correction were performed. Transcripts less than 2-fold differentially expressed at 346 99% confidence in all pairwise comparisons (22,888 transcripts) were removed from the analysis. 347 Additionally, 167 transcripts that were consistently more highly expressed in odd-numbered leaf 348 primordia (1.5 fold higher than immediately preceding and succeeding even-numbered primordia) 349 were removed from analysis. Leaves to be used as standards in juvenile (1-3) and adult (9-11) 350 comparisons were selected based on morphological indicators and genome-wide comparisons. 351 Genes that were at least 2-fold differentially expressed at 99% confidence in nine comparisons 352 (leaves 1, 2, and 3 compared to leaves 9, 10, and 11) or at least 5-fold differentially expressed in 353 six comparisons (leaves 1 and 2 compared to leaves 9, 10, and 11) were considered to be juvenile 354 or adult-specific. Pearson hierarchical clustering was performed using Arraystar. 355 Gene ontology analysis 356 Singular Enrichment Analysis was performed using AgriGO (Du et al 2010). Gene sets were 357 queried against the Zea mays V5a reference set using standard settings (Fisher’s exact test with 358 significance threshold of 0.05, Yekutieli multi-test adjustment). 359 Pathway visualization 360 Differentially expressed genes were visualized in Mapman (Thimm et al 2004) using the 2012 361 B73 genome mapping. The difference in expression between leaf primordia one and nine was 362 used for visualization and for Benjamini-Hochberg corrected Wilcoxon sum rank tests. 363 Promoter motif analysis 364 Enriched promoter sequences (motifs) were identified using SCOPE (Chakravarty et al 2007) and 365 MEME (Bailey and Elkan 1994). Motifs were compared to transcription factor binding site 366 sequences in the 2014 JASPAR plant database (Mathelier et al 2014) using TOMTOM (Gupta et 367 al 2007). 368 Seedling treatment and scoring 369 Emerging seedlings (first leaf partially expanded) received a single application of 100µl of 370 varying concentrations of jasmonic acid (Cayman Chemical, aqueous solution), salicylic acid 371



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(Sigma Life Science, 40% ethanol solution), or hydrogen peroxide (Sigma Life Science, aqueous 372 solution) to the apical whorl, which serves as a natural funnel. Mock treatments consisted of 373 application of the same volume of solute. 25mM JA treatment caused ~20% mortality while 374 50mM JA killed all treated seedlings. Additional treatments with JA occurred at 2-day intervals. 375 Leaves were examined for the presence and density of macrohairs once fully expanded. 376 Epidermal cell wall characters (presence or absence of lignin, degree of cell wall crenulation, 377 presence of bulliform cells) were scored from peels stained with Toluidine Blue-O. 378



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379 380 Acknowledgments 381 We thank Abby Long for help with the microarray experiments. We are grateful to the reviewers 382 for their thoughtful comments. This work was supported by NSF 0820562. BB was also 383 supported by Avis Cone Summer Fellowships. 384 385 Author Contributions 386 B. B. carried out most of the experiments, conducted data analysis, designed JA treatment, and 387 wrote the first draft. 388 K.O. conducted the multiple JA treatment experiments and microscopy. 389 C. L. C. consulted on experimental design, interpretation of data, and edited the ms. 390 J. R. M. hosted microarray hybridization, consulted on data analysis, and edited the ms. 391 E. E. I. designed the experiments and wrote the ms. 392 393



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395 396 397 Table 1. Biological process gene ontology of juvenile and adult subclusters, ranked by p value. 398 The juvenile cluster was further subdivided by those genes strongly upregulated in leaves 1 and 2 399 only vs. those upregulated in all four juvenile samples. Fisher’s exact test after multiple testing 400 correction was used to generate the P values. Enrichment represents the ratio of percentage in set 401 compared to percentage in reference. 402 403

Wilcoxon sum-rank tests of Mapman categories p-value Phase (J/A)Major categories ("bins")Photosynthesis 4.39E-30 JuvenileSecondary metabolism 8.39E-12 JuvenileCell 2.76E-08 AdultAmino acid metabolism 4.72E-07 JuvenileCell wall 2.18E-06 JuvenileTetrapyrrole synthesis 2.34E-06 JuvenileRNA 4.35E-06 AdultDNA 5.16E-05 AdultMetal handling 3.16E-03 JuvenileTranscription factor familiesSBP,Squamosa promoter binding protein family 4.81E-04 AdultB3 transcription factor family 6.61E-04 AdultMADS box transcription factor family 7.75E-04 AdultC2C2(Zn) GATA transcription factor family 1.91E-03 JuvenileCCAAT box binding factor family, HAP2 6.50E-03 AdultChromatin Remodeling Factors 1.14E-02 AdultARF, Auxin Response Factor family 1.43E-02 AdultC2C2(Zn) YABBY family 1.61E-02 AdultGRAS transcription factor family 1.84E-02 JuvenileC2C2(Zn) CO-like, Constans-like zinc finger family 1.95E-02 Juvenile



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404 405 Table 2: Mapman bins differing most greatly between leaf primordia 1 and 9. P-value indicates 406 the false discovery rate after multiple testing correction. 407 408

Significant GO process terms p value EnrichmentJuvenile Photosynthesis 7.8e-16 10.8Oxidation reduction 4.1e-08 2.0Immune system process 0.00013 3.2Lipid metabolic process 0.00011 2.2Inorganic anion transport 0.00073 4.7 Early juvenile cluster Oxidation reduction 2.9e-15 2.0Response to stress 8.9e-07 1.6Temperature homeostasis 2.6e-06 1.7Oligopeptide transport 2.2e-06 4.3Metal ion transport 0.00034 1.9 Full juvenile cluster Photosynthesis 1.9e-18 8.5Tetrapyrrole biosynthetic process 7.5e-08 7.5Protein folding 1.6e-05 2.4Translation 0.00012 1.6Adult Regulation of transcription 1.1e-06 2.5Transcription, DNA-dependent 0.00096 2.2



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Figure Legends 409 Figure 1: Genome-wide differences in gene expression among plastochron 6 leaf primordia. A. 410 Pairwise comparisons of genome-wide 8mm leaf primordia expression (Pearson r2), with red hue 411 increasing with difference. B. Hierarchical clustering of leaf primordia 1-12 using 16,772 412 differentially expressed transcripts. C. Pearson hierarchical clustering in Arraystar of 16,772 413 variably expressed transcripts, normalized to leaf one. Major juvenile and adult phase-specific 414 clusters are indicated. Per row color scale excludes highest and lowest 1% of values. Red color 415 indicates highest expression and blue lowest. 416 Figure 2. Pearson hierarchical clustering in Arraystar of 3,385 juvenile cluster transcripts. EJ and 417 FJ indicate constituents of early juvenile and full juvenile clusters respectively. Transcripts of 418 miR156 loci located as indicated. Per row color scale excludes highest and lowest 1% of values. 419 Red color indicates highest expression and blue lowest. 420 Figure 3. Adult upregulated transcripts include those for SPB’s and are co-expressed with 421 miR172c. 422 Figure 4. Promoter motifs found in the upstream 400bp of transcripts most closely co-expressed 423 with A. miR156f/g/i or B. miR172c. The 10 most enriched motifs identified by the SCOPE and 424 DREME programs were queried against known binding sequences in TOMTOM and with hits 425 with q value ≤ 0.1 (indicating the minimum false discovery rate which would include the hit) are 426 presented. All motifs except ACGTRS originate from DREME. 427 Figure 5. Juvenile specific co-expression of miR156 with selected JA and SA-associated 428 transcripts, normalized to leaf 1 expression. 429 Figure 6. JA effects on phase-specific leaf traits. A-F. Phase-specific traits. A. No trichomes on 430 juvenile leaves. B. Trichomes on adult leaves. C.-F. Toluidine Blue O (TBO) stained epidermal 431 peals. C. Juvenile. D. Transition E. Adult F. Bulliform cells (adult). G. A single treatment of 432



21

increasing concentrations of JA at seedling emergence increasingly reduced the area with 433 trichomes and final length of leaf 5, the first transition leaf. n=10. H. Increasing doses of 5 mM 434 JA, 2 days apart, delayed appearance of adult traits in leaf 6. n=12 I. Leaf 6 of JA-deficient 435 tasselseed 1 mutants develop adult-specific trichomes earlier than w.t. sibs. n=8. Mutant leaf 6 436 stained entirely blue with TBO with adult-type crenulation (not shown). J. Hierarchical 437 clustering using combined juvenile and adult-specific sets of genes. JA-treated leaf 5 (5JA) 438 clusters with leaves 3 and 4; untreated leaf 5 clusters with adult leaves. 439 Figure 7. Leaf primordium expression patterns for A. selected redox and stress transcripts from 440 the early juvenile cluster and B. selected redox and photosynthetic transcripts co-expressed with 441 miR156f/g/i loci. Per row color scale excludes highest and lowest 1% of values. Red color 442 indicates highest expression and blue lowest. 443 Supplemental Table 1. Phase specific transcripts. Difference in expression levels of dynamic 444 transcripts between leaf primordia 1 and 9. 445 Supplemental Table 2. Selected genes showing change in expression in leaf 5 primordia in 446 response to JA treatment compared to untreated leaf 5. 447 Supplemental Figure 1. Treatment of seedlings with, A) SA or, B) hydrogen peroxide. Error 448 bars represent standard deviation of irregular sector. * indicates significant difference in 449 percentage of leaf hairless compared to all other treatments at p<0.05, Student’s t-test. 450

451 452

453



22

Literature Cited 454 Achard P, Renou JP, Berthomé R, Harberd NP, Genschik P. (2008) Plant DELLAs restrain 455 growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr 456 Biol. 18:656-60 457 Acosta IF, Lappara H, Romera SP, Schmelz E, Hamberg M, Mottinger JP, Moreno MA, 458 Dellaporta SL. (2009) tasselseed1 is a lipoxygenase affecting jasmonic acid signaling in sex 459 determination of maize. Science 323: 262-265 460 Baena-González E, Rolland F, Thevelein JM, Sheen J. (2007) A central integrator of transcription 461 networks in plant stress and energy signalling. Nature. 23;448(7156):938-42. 462 Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D. (2009) 463 Control of Arabidopsis meristem development by thioredoxin-dependent regulation of 464 intercellular transport. Proc Natl Acad Sci USA 106:3615-20 465 Birkenbihl RP, Jach G, Saedler H, Huijser P. (2005) Functional dissection of the plant-specific 466 SBP-domain: overlap of the DNA-binding and nuclear localization domains. J Mol Biol. 467 352:585-96 468 Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W. (2010) Sugar 469 signalling and antioxidant network connections in plant cells. FEBS J. 277:2022-37 470 Bolouri-Moghaddam MR, Van den Ende W. (2012) Sugars and plant innate immunity. J Exp Bot. 471 63:3989-98 472 Cambier V, Hance T, de Hoffmann E. (2000) Variation of DIMBOA and related compounds 473 content in relation to the age and plant organ in maize. Phytochemistry 53:223-9 474 Chen JH, Jiang HW, Hsieh EJ, Chen HY, Chien CT, Hsieh HL, Lin TP. (2012) Drought and salt 475 stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to 476 the combined effect of glutathione and abscisic acid. Plant Physiol. 2012 158:340-51 477 Cho HJ, Kim JJ, Lee JH, Kim W, Jung JH, Park CM, Ahn JH. (2012A) SHORT VEGETATIVE 478 PHASE (SVP) protein negatively regulates miR172 transcription via direct binding to the pri-479 miR172a promoter in Arabidopsis. FEBS Lett. 586:2332-7. 480



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Dynamic Transcripts (16,772)

Leaf 1 2 3 4 5 6 7 8 9 10 11 12

1 1 0.94 0.71 0.64 0.67 0.59 0.56 0.58 0.56 0.53 0.54 0.55

2 0.98 1 0.84 0.79 0.79 0.74 0.72 0.73 0.70 0.68 0.69 0.69

3 0.90 0.95 1 0.94 0.83 0.87 0.87 0.86 0.83 0.84 0.83 0.80

4 0.88 0.93 0.97 1 0.81 0.90 0.87 0.90 0.84 0.88 0.85 0.87

5 0.89 0.93 0.94 0.93 1 0.90 0.91 0.89 0.91 0.85 0.87 0.84

6 0.87 0.92 0.95 0.96 0.96 1 0.96 0.97 0.95 0.96 0.96 0.94

7 0.85 0.91 0.96 0.95 0.97 0.98 1 0.95 0.96 0.95 0.95 0.90

8 0.86 0.91 0.95 0.96 0.96 0.99 0.98 1 0.96 0.96 0.96 0.96

9 0.86 0.90 0.94 0.94 0.97 0.98 0.98 0.98 1 0.96 0.96 0.92

10 0.84 0.89 0.94 0.96 0.94 0.98 0.98 0.98 0.98 1 0.98 0.95

11 0.85 0.90 0.94 0.95 0.95 0.98 0.98 0.98 0.98 0.99 1 0.96

12 0.85 0.90 0.93 0.95 0.94 0.98 0.96 0.98 0.97 0.98 0.99 1

All Transcripts (39,827)

A

B

Leaf 1 2 3 4 5 6 8 10 11 9 7 12

Figure 1



C Leaf 1 2 3 4 5 6 7 8 9 10 11 12

Juvenile

Adult

Figure 1

Figure 1: Genome-wide differences in gene expression among plastochron 6 leaf primordia. A Pairwise comparisons of genome-wide 8mm leaf primordial expression (Pearson r2), with red hue increasing with difference. B Hierarchical clustering of leaf primordia 1-12 using 16,772 differentially expressed transcripts. C. Pearson hierarchical clustering in Arraystar of 16,772 variably expressed transcripts, normalized to leaf one. Major juvenile and adult phase-specific clusters are indicated. Per row color scale excludes highest and lowest 1% of values. Red color indicates highest expression and blue lowest.



*miR156h

*miR156e

*miR156i

*miR156f/g

*miR156l

EJ

FJ

1 2 3 4 5 6 7 8 9 10 11 12 Leaf

Figure 2

Figure 2. Pearson hierarchical clustering in Arraystar of 3,385 juvenile cluster transcripts. EJ and FJ indicate constituents of early juvenile and full juvenile clusters. Transcripts of miR156 loci located as indicated. Per row color scale excludes highest and lowest 1% of values. Red color indicates highest expression and blue lowest.



leaf 1 2 3 4 5 6 7 8 9 10 11 12

Figure 3

Figure 3. Adult upregulated transcripts include those for SPB’s and are co-expressed with miR172c



Figure 4

Figure 4. Promoter motifs found in the upstream 400bp of transcripts most closely co-expressed with A. miR156f/g/i or B. miR172c. The 10 most enriched motifs identified by the SCOPE and DREME programs were queried against known binding sequences in TOMTOM and with hits with q value ≤ 0.1 (indicating the minimum false discovery rate which would include the hit) are presented. All motifs except ACGTRS originate from DREME.



Figure 5

Figure 5. Leaf primordium expression patterns for A. selected redox and stress transcripts from the early juvenile cluster and B. selected redox and photosynthetic transcripts co-expressed with miR156f/g/i loci. Per row color scale excludes highest and lowest 1% of values. Red color indicates highest expression and blue lowest.

A B



Figure 6

H G

Figure 6. JA effects on phase-specific leaf traits. A-F. Phase-specific traits. A. No trichomes on juvenile leaves. B. Trichomes on adult leaves. C.-F. Toluidine Blue O (TBO) stained epidermal peals. C. Juvenile. D. Transition E. Adult F. Bulliform cells (adult). G. A single treatment of increasing concentrations of JA at seedling emergence increasingly reduced the area with trichomes and final length of leaf 5, the first transition leaf. n=10. H. Increasing doses of 5 mM JA, 2 days apart, delayed appearance of adult traits in leaf 6. n=12 C. Leaf 6 of JA-deficient tasselseed 1 mutants develop adult-specific trichomes earlier than w.t. sibs. n=8. I. Mutant leaf 6 stained entirely blue with TBO with adult crenulation (not shown) J. Hierarchical clustering using combined juvenile and adult-specific sets of genes. JA-treated leaf 5 (5JA) clusters with leaves 3 and 4; untreated leaf 5 clusters with adult leaves.

A B C D E F

I

J

1 2 3 4 5JA 5 6 8 7 9 10 11 12



Figure 7

Figure 7. Expression patterns for A. selected redox and stress transcripts from the early juvenile cluster and B. selected redox and photosynthetic transcripts co-expressed with miR156f/g/i loci. Per row color scale excludes highest and lowest 1% of values. Red color indicates highest expression and blue lowest.

A B



Parsed CitationsAchard P, Renou JP, Berthomé R, Harberd NP, Genschik P. (2008) Plant DELLAs restrain growth and promote survival of adversityby reducing the levels of reactive oxygen species. Curr Biol. 18:656-60

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Acosta IF, Lappara H, Romera SP, Schmelz E, Hamberg M, Mottinger JP, Moreno MA, Dellaporta SL. (2009) tasselseed1 is alipoxygenase affecting jasmonic acid signaling in sex determination of maize. Science 323: 262-265


Baena-González E, Rolland F, Thevelein JM, Sheen J. (2007) A central integrator of transcription networks in plant stress andenergy signalling. Nature. 23;448(7156):938-42.


Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D. (2009) Control of Arabidopsis meristemdevelopment by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci USA 106:3615-20


Birkenbihl RP, Jach G, Saedler H, Huijser P. (2005) Functional dissection of the plant-specific SBP-domain: overlap of the DNA-binding and nuclear localization domains. J Mol Biol. 352:585-96


Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W. (2010) Sugar signalling and antioxidant networkconnections in plant cells. FEBS J. 277:2022-37


Bolouri-Moghaddam MR, Van den Ende W. (2012) Sugars and plant innate immunity. J Exp Bot. 63:3989-98Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Cambier V, Hance T, de Hoffmann E. (2000) Variation of DIMBOA and related compounds content in relation to the age and plantorgan in maize. Phytochemistry 53:223-9


Chen JH, Jiang HW, Hsieh EJ, Chen HY, Chien CT, Hsieh HL, Lin TP. (2012) Drought and salt stress tolerance of an Arabidopsisglutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. PlantPhysiol. 2012 158:340-51


Cho HJ, Kim JJ, Lee JH, Kim W, Jung JH, Park CM, Ahn JH. (2012A) SHORT VEGETATIVE PHASE (SVP) protein negativelyregulates miR172 transcription via direct binding to the pri-miR172a promoter in Arabidopsis. FEBS Lett. 586:2332-7.


Chuck G, Cigan AM, Saeteurn K, Hake S. (2007) The heterochronic maize mutant Corngrass1 results from overexpression of atandem microRNA. Nat Genet. 239:544-9


Chuck G, Whipple C, Jackson D, Hake S. (2010) The maize SBP-box transcription factor encoded by tasselsheath4 regulates bractdevelopment and the establishment of meristem boundaries. Development 137:1243-50


Courteille A., Vesa S., Sanz-Barrio R., Cazale A. C., Becuwe-Linka N., Farran I., et al. (2013). Thioredoxin m4 controlsphotosynthetic alternative electron pathways in Arabidopsis. Plant Physiol. 161: 508-520



http://www.ncbi.nlm.nih.gov/pubmed?term=%28Curr Biol%5BTitle%5D%29 AND 18%5BVolume%5D AND 656%5BPagination%5D AND Achard P%2C Renou JP%2C Berthom� R%2C Harberd NP%2C Genschik P%2E%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Achard&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiology%5BTitle%5D%29 AND 108%5BVolume%5D AND 475%5BPagination%5D AND Evans MM%2C Poethig RS%2E%5BAuthor%5D&dopt=abstract

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Tomé F, Nägele T, Adamo M, Garg A, Marco-Llorca C, Nukarinen E, Pedrotti L, Peviani A, Simeunovic A, Tatkiewicz A, Tomar M,Gamm M. (2014) The low energy signaling network. Front Plant Sci. 17;5:353.


Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T, Franke A, Feil R, Lunn JE, Stitt M, Schmid M. (2013) Regulation offlowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339:704-7


Wang JW, Czech B, Weigel D. (2009a) miR156-regulated SPL transcription factors define an endogenous flowering pathway inArabidopsis thaliana. Cell 138:738-49


Wang Y, Hu Z, Yang Y, Chen X, Chen G. (2009b) Function annotation of an SBP-box gene in Arabidopsis based on analysis of co-expression networks and promoters. Int J Mol Sci. 10:116-32


Wild M, Davière JM, Cheminant S, Regnault T, Baumberger N, Heintz D, Baltz R, Genschik P, Achard P. (2012) The ArabidopsisDELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell 24:3307-19


Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS. (2009) The sequential action of miR156 and miR172 regulatesdevelopmental timing in Arabidopsis. Cell 138:750-9


Xiang L, Li Y, Rolland F, Van den Ende W. (2011) Neutral invertase, hexokinase and mitochondrial ROS homeostasis: emerginglinks between sugar metabolism, sugar signaling and ascorbate synthesis. Plant Signal Behav. 6:1567-73


Yadav UP, Ivakov A, Feil R, Duan GY, Walther D, Giavalisco P, Piques M, Carillo P, Hubberten HM, Stitt M, Lunn JE. (2014) Thesucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J Exp Bot. 65:1051-68


Yamada K, Hara-Nishimura I, Nishimura M. (2011) Unique defense strategy by the endoplasmic reticulum body in plants. Plant CellPhysiology 52:2039-49


Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner D. (2009) The microRNA-regulated SBP-Box transcription factor SPL3 isa direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell. 17:268-78


Yamamoto H, Peng L, Fukao Y, Shikanai T. (2011) An Src homology 3 domain-like fold protein forms a ferredoxin binding site forthe chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Cell 23: 1480-93.

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Development%5BTitle%5D%29 AND 110%5BVolume%5D AND 985%5BPagination%5D AND Sylvester A W%2C Cande W Z%2C and Freeling M%5BAuthor%5D&dopt=abstract

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Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T. (2009) SQUAMOSA Promoter Binding Protein-Like7 Is a CentralRegulator for Copper Homeostasis in Arabidopsis. Plant Cell. 21:347-61


Yan J, Niu F, Liu WZ, Zhang H, Wang B, Yang B, Jiang YQ. (2014) Arabidopsis CIPK14 positively regulates glucose response.Biochem Biophys Res Commun. 450:1679-83.


Yang L, Conway SR, Poethig RS. (2011) Vegetative phase change is mediated by a leaf-derived signal that represses thetranscription of miR156. Development 138:245-9.


Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, Li Q, Xiao LT, Sun TP, Li J, Deng XW, Lee CM, Thomashow MF, Yang Y, He Z, He SY.(2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl AcadSci U S A. 109:E1192-200


Yang L, Xu M, Koo Y, He J, Poethig RS. (2013) Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing theexpression of MIR156A and MIR156C. Elife. 2:260


Yu S, Cao L, Zhou CM, Zhang TQ, Lian H, Sun Y, Wu J, Huang J, Wang G, Wang JW. (2013) Sugar is an endogenous cue forjuvenile-to-adult phase transition in plants. Elife 2:269


Yu S, Galvão VC, Zhang YC, Horrer D, Zhang TQ, Hao YH, Feng YQ, Wang S, Schmid M, Wang JW. (2012) Gibberellin regulates theArabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors. Plant Cell 24:3320-32


Zaffagnini M, Fermani S, Costa A, Lemaire SD, Trost P. (2013) Plant cytoplasmic GAPDH: redox post-translational modifications andmoonlighting properties.Front Plant Sci. 4:450


Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RA, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ. (2009)Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. PlantPhysiology 14:1860-71


Zhu QH, Helliwell CA. (2011) Regulation of flowering time and floral patterning by miR172. J Exp Bot. 62:487-95Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title


http://search.crossref.org/?page=1&rows=2&q=Yamamoto H, Peng L, Fukao Y, Shikanai T. (2011) An Src homology 3 domain-like fold protein forms a ferredoxin binding site for the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Cell 23: 1480-93.

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 21%5BVolume%5D AND 347%5BPagination%5D AND Yamasaki H%2C Hayashi M%2C Fukazawa M%2C Kobayashi Y%2C Shikanai T%2E%5BAuthor%5D&dopt=abstract

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Plant Physiology Preview. Published on June 15, 2016, as ... · 12 Department of Biology,...

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