The dehydration stress of couch grass is associated with its lipid metabolism, the induction of transporters and the re-programming of development coordinated by ABA
Language English Country England, Great Britain Media electronic
Document type Journal Article
Grant support
QH81287 and QJ1310055
Czech National Agency for Agricultural Research
LO1417
Czech ministry of Education Youth and Sports
MSMT 20/2015
Specific University Research
RO0417
Czech Ministry of Agriculture
PubMed
29720087
PubMed Central
PMC5930771
DOI
10.1186/s12864-018-4700-3
PII: 10.1186/s12864-018-4700-3
Knihovny.cz E-resources
- Keywords
- Barley, Couch grass, Crown, Dehydration stress, Drought, Microarray, Rhizome,
- MeSH
- Electrolytes metabolism MeSH
- Stress, Physiological genetics MeSH
- Abscisic Acid metabolism MeSH
- Poaceae genetics metabolism physiology MeSH
- Membrane Transport Proteins genetics MeSH
- Lipid Metabolism genetics MeSH
- Droughts * MeSH
- Gene Expression Profiling MeSH
- Water metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Electrolytes MeSH
- Abscisic Acid MeSH
- Membrane Transport Proteins MeSH
- Water MeSH
BACKGROUND: The wild relatives of crop species represent a potentially valuable source of novel genetic variation, particularly in the context of improving the crop's level of tolerance to abiotic stress. The mechanistic basis of these tolerances remains largely unexplored. Here, the focus was to characterize the transcriptomic response of the nodes (meristematic tissue) of couch grass (a relative of barley) to dehydration stress, and to compare it to that of the barley crown formed by both a drought tolerant and a drought sensitive barley cultivar. RESULTS: Many of the genes up-regulated in the nodes by the stress were homologs of genes known to be mediated by abscisic acid during the response to drought, or were linked to either development or lipid metabolism. Transporters also featured prominently, as did genes acting on root architecture. The resilience of the couch grass node arise from both their capacity to develop an altered, more effective root architecture, but also from their formation of a lipid barrier on their outer surface and their ability to modify both their lipid metabolism and transporter activity when challenged by dehydration stress. CONCLUSIONS: Our analysis revealed the nature of dehydration stress response in couch grass. We suggested the tolerance is associated with lipid metabolism, the induction of transporters and the re-programming of development coordinated by ABA. We also proved the applicability of barley microarray for couch grass stress-response analysis.
See more in PubMed
Beddington J, Asaduzzaman M, Fernandez A, Clark M, Guillou M, Jahn M, et al. Achieving food security in the face of climate change: summary for policy makers from the commission on sustainable agriculture and climate change. Copenhagen: CGIAR Research Program on Climate Change; 2011.
Devendra C. Climate change threats and effects: challenges for agriculture and food security. Kuala Lumpur: Academy of Sciences Malaysia; 2012.
Field CB, editor. Managing the risks of extreme events and disasters to advance climate change adaptation: special report of the intergovernmental panel on climate change. Cambridge: Cambridge University Press; 2012.
Reidy ME, Swanton CJ. Quackgrass. In OMAF factsheet. Ministry of Agriculture, Food and Rural Affairs. 1993. http://www.omafra.gov.on.ca/english/crops/facts/quackgrass.htm. Accesed 1 June 1993.
Fahleson J, Okori P, Åkerblom-Espeby L, Dixelius C. Genetic variability and genomic divergence of Elymus repens and related species. Plant Syst Evol. 2008;271(3–4):143–156. doi: 10.1007/s00606-007-0623-1. DOI
Mahelka V. On the origin and hybridization of polyploid wheatgrasses - on the trail of cryptic progenitors. Živa. 2013;61(4):149–153.
Mason-Gamer RJ. Phylogeny of a genomically diverse group of Elymus (Poaceae) allopolyploids reveals multiple levels of reticulation. PLoS One. 2013;8(11):e78449. doi: 10.1371/journal.pone.0078449. PubMed DOI PMC
Zhang T, Zhao X, Huang L, Liu X, Zong Y, Zhu L, et al. Tissue-specific transcriptomic profiling of sorghum propinquum using a rice genome array. PLoS One. 2013;8(3):e60202. doi: 10.1371/journal.pone.0060202. PubMed DOI PMC
Horvath DP, Schaffer R, West M, Wisman E. Arabidopsis microarrays identify conserved and differentially expressed genes involved in shoot growth and development from distantly related plant species. Plant J. 2003;34(1):125–134. doi: 10.1046/j.1365-313X.2003.01706.x. PubMed DOI
Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, et al. Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol. 2004;135(3):1697–1709. doi: 10.1104/pp.104.039909. PubMed DOI PMC
Weber M, Harada E, Vess C, Roepenack-Lahaye EV, Clemens S. Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J. 2004;37(2):269–281. doi: 10.1046/j.1365-313X.2003.01960.x. PubMed DOI
Yang SS, Valdés-López O, Xu WW, Bucciarelli B, Gronwald JW, Hernández G, et al. Transcript profiling of common bean (Phaseolus vulgaris L.) using the GeneChip® soybean genome Array: optimizing analysis by masking biased probes. BMBMC Plant Biol. 2010;10(1):85. doi: 10.1186/1471-2229-10-85. PubMed DOI PMC
Bagnaresi P, Moschella A, Beretta O, Vitulli F, Ranalli P, Perata P. Heterologous microarray experiments allow the identification of the early events associated with potato tuber cold sweetening. BMC Genomics. 2008;9(1):176. doi: 10.1186/1471-2164-9-176. PubMed DOI PMC
Moore S, Payton P, Wright M, Tanksley S, Giovannoni J. Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae. J Exp Bot. 2005;56(421):2885–2895. doi: 10.1093/jxb/eri283. PubMed DOI
Ponce-Valadez M, Fellman SM, Giovannoni J, Gan SS, Watkins CB. Differential fruit gene expression in two strawberry cultivars in response to elevated CO 2 during storage revealed by a heterologous fruit microarray approach. Postharvest Biol Tec. 2009;51(2):131–140. doi: 10.1016/j.postharvbio.2008.08.001. DOI
Svoboda P, Janská A, Spiwok V, Prášil IT, Kosová K, Vítámvás P, Ovesná J. Global scale transcriptional profiling of two contrasting barley genotypes exposed to moderate drought conditions: contribution of leaves and crowns to water shortage coping strategies. Front Plant Sci. 2016;7:1958. doi: 10.3389/fpls.2016.01958. PubMed DOI PMC
Kosová K, Vítámvás P, Prášil IT. Wheat and barley dehydrins under cold, drought, and salinity–what can LEA-II proteins tell us about plant stress response? Front Plant Sci. 2014;5:343. PubMed PMC
Baduel P, Arnold B, Weisman CM, Hunter B, Bomblies K. Habitat-associated life history and stress-tolerance variation in Arabidopsis arenosa. Plant Physiol. 2016;171(1):437–451. doi: 10.1104/pp.15.01875. PubMed DOI PMC
Hirano T, Matsuzawa T, Takegawa K, Sato MH. Loss-of-function and gain-of-function mutations in FAB1A/B impair endomembrane homeostasis, conferring pleiotropic developmental abnormalities in Arabidopsis. Plant Physiol. 2011;155(2):797–807. doi: 10.1104/pp.110.167981. PubMed DOI PMC
Stührwohldt N, Dahlke RI, Steffens B, Johnson A, Sauter M. Phytosulfokine-α controls hypocotyl length and cell expansion in Arabidopsis thaliana through phytosulfokine receptor 1. PLoS One. 2011;6(6):e21054. doi: 10.1371/journal.pone.0021054. PubMed DOI PMC
Chen YE, Liu WJ, Su YQ, Cui JM, Zhang ZW, Yuan M, et al. Different response of photosystem II to short and long-term drought stress in Arabidopsis thaliana. Physiol Plantarum. 2016;158(2):225–235. doi: 10.1111/ppl.12438. PubMed DOI
Horvath D. Genomics for weed science. Curr Genomics. 2010;11(1):47–51. doi: 10.2174/138920210790217972. PubMed DOI PMC
Horvath D. Recent genomic advances for weed science. In: Ch N, editor. Advances in genome science: keeping up with genome sequence and expression: Sharjah: Bentham Science Publishers; 2014. p. 127–42.
Mikulka J, Kneifelová M. Vegetative reproduction of Cirsium arvense (l.) scop., Sonchus arvensis l., Stachys palustris l., Polygonum amphibium l. and Elytrigia repens (l.) desv. AcActa Herb. 2004;13(1):137–178.
Qin X, Zeevaart JA. The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Nat Acad Sci USA. 1999;96(26):15354–15361. doi: 10.1073/pnas.96.26.15354. PubMed DOI PMC
Rohila JS, Jain RK, Wu R. Genetic improvement of basmati rice for salt and drought tolerance by regulated expression of a barley Hva1 cDNA. Plant Sci. 2002;163(3):525–532. doi: 10.1016/S0168-9452(02)00155-3. DOI
Bahieldin A, Mahfouz HT, Eissa HF, Saleh OM, Ramadan AM, Ahmed IA, et al. Field evaluation of transgenic wheat plants stably expressing the HVA1 gene for drought tolerance. Physiol Plantarum. 2005;123(4):421–427. doi: 10.1111/j.1399-3054.2005.00470.x. DOI
Fu D, Huang B, Xiao Y, Muthukrishnan S, Liang GH. Overexpression of barley hva1 gene in creeping bentgrass for improving drought tolerance. Plant Cell Rep. 2007;26(4):467–477. doi: 10.1007/s00299-006-0258-7. PubMed DOI
Checker VG, Chhibbar AK, Khurana P. Stress-inducible expression of barley Hva1 gene in transgenic mulberry displays enhanced tolerance against drought, salinity and cold stress. Transgenic Res. 2012;21(5):939–957. doi: 10.1007/s11248-011-9577-8. PubMed DOI
Lal S, Gulyani V, Khurana P. Overexpression of HVA1 gene from barley generates tolerance to salinity and water stress in transgenic mulberry (Morus indica) Transgenic Res. 2008;17(4):651. doi: 10.1007/s11248-007-9145-4. PubMed DOI
Nguyen TX, Sticklen M. Barley HVA1 gene confers drought and salt tolerance in transgenic maize (Zea mays L.) Adv Crop Sci Tech. 2013;1(105):2.
Takahashi R, Joshee N, Kitagawa Y. Induction of chilling resistance by water stress, and cDNA sequence analysis and expression of water stress-regulated genes in rice. Plant Mol Biol. 1994;26(1):339–352. doi: 10.1007/BF00039544. PubMed DOI
Joshee N, Kisaka H, Kitagawa Y. Isolation and characterization of a water stress-specific genomic gene, pwsi 18, from rice. Plant Cell Physiol. 1998;39(1):64–72. doi: 10.1093/oxfordjournals.pcp.a029290. PubMed DOI
Shobbar ZS, Oane R, Gamuyao R, De Palma J, Malboobi MA, Karimzadeh G, et al. Abscisic acid regulates gene expression in cortical fiber cells and silica cells of rice shoots. New Phytol. 2008;178(1):68–79. doi: 10.1111/j.1469-8137.2007.02365.x. PubMed DOI
Piatkowski D, Schneider K, Salamini F, Bartels D. Characterization of five abscisic acid-responsive cDNA clones isolated from the desiccation-tolerant plant Craterostigma plantagineum and their relationship to other water-stress genes. Plant Physiol. 1990;94(4):1682–1688. doi: 10.1104/pp.94.4.1682. PubMed DOI PMC
Hare PD, Cress WA, Van Staden J. Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 1998;21(6):535–553. doi: 10.1046/j.1365-3040.1998.00309.x. DOI
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, et al. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 2002;31(3):279–292. doi: 10.1046/j.1365-313X.2002.01359.x. PubMed DOI
Rösti J, Barton CJ, Albrecht S, Dupree P, Pauly M, Findlay K, et al. UDP-glucose 4-epimerase isoforms UGE2 and UGE4 cooperate in providing UDP-galactose for cell wall biosynthesis and growth of Arabidopsis thaliana. Plant Cell. 2007;19(5):1565–1579. doi: 10.1105/tpc.106.049619. PubMed DOI PMC
Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, et al. Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol. 2003;133(4):1755–1767. doi: 10.1104/pp.103.025742. PubMed DOI PMC
Ge LF, Chao DY, Shi M, Zhu MZ, Gao JP, Lin HX. Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta. 2008;228(1):191–201. doi: 10.1007/s00425-008-0729-x. PubMed DOI
Jang IC, Oh SJ, Seo JS, Choi WB, Song SI, Kim CH, et al. Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol. 2003;131(2):516–524. doi: 10.1104/pp.007237. PubMed DOI PMC
Valliyodan B, Nguyen HT. Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol. 2006;9(2):189–195. doi: 10.1016/j.pbi.2006.01.019. PubMed DOI
Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, et al. Important roles of drought-and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 2002;29(4):417–426. doi: 10.1046/j.0960-7412.2001.01227.x. PubMed DOI
Nishizawa A, Yabuta Y, Shigeoka S. Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 2008;147(3):1251–1263. doi: 10.1104/pp.108.122465. PubMed DOI PMC
Zhu B, Su J, Chang M, Verma DPS, Fan YL, Wu R. Overexpression of a Δ 1-pyrroline-5-carboxylate synthetase gene and analysis of tolerance to water-and salt-stress in transgenic rice. Plant Sci. 1998;139(1):41–48. doi: 10.1016/S0168-9452(98)00175-7. DOI
Kishor PK, Hong Z, Miao GH, Hu CAA, Verma DPS. Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol. 1995;108(4):1387–1394. doi: 10.1104/pp.108.4.1387. PubMed DOI PMC
Anderberg RJ, Walker-Simmons MK. Isolation of a wheat cDNA clone for an abscisic acid-inducible transcript with homology to protein kinases. Proc Natl Acad Sci U S A. 1992;89(21):10183–10187. doi: 10.1073/pnas.89.21.10183. PubMed DOI PMC
Holappa LD, Walker-Simmons MK. The wheat abscisic acid-responsive protein kinase mRNA, PKABA1, is up-regulated by dehydration, cold temperature, and osmotic stress. Plant Physiol. 1995;108(3):1203–1210. doi: 10.1104/pp.108.3.1203. PubMed DOI PMC
Ozturk ZN, Talamé V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, et al. Monitoring large-scale changes in transcript abundance in drought-and salt-stressed barley. Plant Mol Biol. 2002;48(5–6):551–573. doi: 10.1023/A:1014875215580. PubMed DOI
Guo P, Baum M, Grando S, Ceccarelli S, Bai G, Li R, et al. Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. J Exp Bot. 2009;60(12):3531–3544. doi: 10.1093/jxb/erp194. PubMed DOI PMC
Ueda A, Shi W, Nakamura T, Takabe T. Analysis of salt-inducible genes in barley roots by differential display. J P Res. 2002;115(2):0119–0130. doi: 10.1007/s102650200017. PubMed DOI
Mikami K, Katagiri T, Iuchi S, Yamaguchi-Shinozaki K, Shinozaki K. A gene encoding phosphatidylinositol-4-phosphate 5-kinase is induced by water stress and abscisic acid in Arabidopsis thaliana. Plant J. 1998;15(4):563–568. doi: 10.1046/j.1365-313X.1998.00227.x. PubMed DOI
Navarre C, Goffeau A. Membrane hyperpolarization and salt sensitivity induced by deletion of PMP3, a highly conserved small protein of yeast plasma membrane. EMBO J. 2000;19(11):2515–2524. doi: 10.1093/emboj/19.11.2515. PubMed DOI PMC
Pearce RS, Houlston CE, Atherton KM, Rixon JE, Harrison P, Hughes MA, et al. Localization of expression of three cold-induced genes, blt101, blt4. 9, and blt14, in different tissues of the crown and developing leaves of cold-acclimated cultivated barley. PlPlant Physiol. 1998;117(3):787–795. doi: 10.1104/pp.117.3.787. PubMed DOI PMC
Goddard NJ, Dunn MA, Zhang L, White AJ, Jack PL, Hughes MA. Molecular analysis and spatial expression pattern of a low-temperature-specific barley gene, blt101. Plant Mol Biol. 1993;23(4):871–879. doi: 10.1007/BF00021541. PubMed DOI
Aroca R, Porcel R, Ruiz-Lozano JM. Regulation of root water uptake under abiotic stress conditions. J ExpBot. 2012;63(1):43–57. PubMed
Chaumont F, Tyerman SD. Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol. 2014;164(4):1600–1618. doi: 10.1104/pp.113.233791. PubMed DOI PMC
Gambetta GA, Fei J, Rost TL, Knipfer T, Matthews MA, Shackel KA, et al. Water uptake along the length of grapevine fine roots: developmental anatomy, tissue-specific aquaporin expression, and pathways of water transport. Plant Physiol. 2013;163(3):1254–1265. doi: 10.1104/pp.113.221283. PubMed DOI PMC
Heinen RB, Ye Q, Chaumont F. Role of aquaporins in leaf physiology. J Exp Bot. 2009;60(11):2971–2985. doi: 10.1093/jxb/erp171. PubMed DOI
Moshelion M, Halperin O, Wallach R, Oren R, Way DA. Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: crop water-use efficiency, growth and yield. Plant Cell Environ. 2014;38(9):1785–1793. doi: 10.1111/pce.12410. PubMed DOI
Lian HL, Yu X, Lane D, Sun WN, Tang ZC, Su WA. Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Res. 2006;16(7):651. doi: 10.1038/sj.cr.7310068. PubMed DOI
Martre P, Morillon R, Barrieu F, North GB, Nobel PS, Chrispeels MJ. Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol. 2002;130(4):2101–2110. doi: 10.1104/pp.009019. PubMed DOI PMC
Olien CR. Freezing stresses and survival. Ann Rev Plant Physio. 1967;18(1):387–408. doi: 10.1146/annurev.pp.18.060167.002131. DOI
Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ. Plant responses to cold: transcriptome analysis of wheat. Plant Biotech J. 2010;8(7):749–771. doi: 10.1111/j.1467-7652.2010.00536.x. PubMed DOI
Byrt CS, Zhao M, Kourghi M, Bose J, Henderson SW, Qiu J, et al. Non selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. Plant Cell Environ. 2017;40(6):802–815. doi: 10.1111/pce.12832. PubMed DOI
Bellati J, Champeyroux C, Hem S, Rofidal V, Krouk G, Maurel C, Santoni V. Novel aquaporin regulatory mechanisms revealed by interactomics. Mol Cell Proteomics. 2016;15(11):3473–3487. doi: 10.1074/mcp.M116.060087. PubMed DOI PMC
Wudick MM, Luu DT, Maurel C. A look inside: localization patterns and functions of intracellular plant aquaporins. New Phytol. 2009;184(2):289–302. doi: 10.1111/j.1469-8137.2009.02985.x. PubMed DOI
Wang LL, Chen AP, Zhong NQ, Liu N, Wu XM, Wang F, et al. The Thellungiella salsuginea tonoplast aquaporin TsTIP1;2 functions in protection against multiple abiotic stresses. Plant Cell Physiol. 2014;55(1):148–161. doi: 10.1093/pcp/pct166. PubMed DOI PMC
Peng Y, Lin W, Cai W, Arora R. Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta. 2007;226(3):729–740. doi: 10.1007/s00425-007-0520-4. PubMed DOI
Lev S. Nonvesicular lipid transfer from the endoplasmic reticulum. CSH Perspect Biol. 2012;4(10):a013300. PubMed PMC
Edstam MM, Blomqvist K, Eklöf A, Wennergren U, Edqvist J. Coexpression patterns indicate that GPI-anchored non-specific lipid transfer proteins are involved in accumulation of cuticular wax, suberin and sporopollenin. Plant Mol Biol. 2013;83(6):625–649. doi: 10.1007/s11103-013-0113-5. PubMed DOI
Endo S, Iwamoto K, Fukuda H. Overexpression and cosuppression of xylem-related genes in an early xylem differentiation stage-specific manner by the AtTED4 promoter. Plant Biotechnol J. 2017; 10.1111/pbi.12784. PubMed PMC
Jasieniecka-Gazarkiewicz K, Lager I, Carlsson A, Gutbrod K, Peisker H, Dörmann P, et al. Acyl-CoA: lysophosphatidylethanolamine acyltransferase activity affects growth. Plant Physiol. 2017; 10.1104/pp.17.00391. PubMed PMC
Guo L, Yang H, Zhang X, Yang S. Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. J Exp Bot. 2013;64(6):1755–1767. doi: 10.1093/jxb/ert040. PubMed DOI PMC
Janská A, Aprile A, Cattivelli L, Zámečník J, de Bellis L, Ovesná J. The up-regulation of elongation factors in the barley leaf and the down-regulation of nucleosome assembly genes in the crown are both associated with the expression of frost tolerance. Funct Integr Genomic. 2014;14(3):493–506. doi: 10.1007/s10142-014-0377-0. PubMed DOI
Jarzyniak KM, Jasiński M. Membrane transporters and drought resistance–a complex issue. Front Plant Sci. 2014;5:687. doi: 10.3389/fpls.2014.00687. PubMed DOI PMC
Kim H, Lee SB, Kim HJ, Min MK, Hwang I, Suh MC. Characterization of glycosylphosphatidylinositol-anchored lipid transfer protein 2 (LTPG2) and overlapping function between LTPG/LTPG1 and LTPG2 in cuticular wax export or accumulation in Arabidopsis thaliana. Plant Cell Physiol. 2012;53(8):1391–1403. doi: 10.1093/pcp/pcs083. PubMed DOI
DeBono A, Yeats TH, Rose JK, Bird D, Jetter R, Kunst L, et al. Arabidopsis LTPG is a glycosylphosphatidylinositol-anchored lipid transfer protein required for export of lipids to the plant surface. Plant Cell. 2009;21(4):1230–1238. doi: 10.1105/tpc.108.064451. PubMed DOI PMC
McFarlane HE, Shin JJ, Bird DA, Samuels AL. Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. Plant Cell. 2010;22(9):3066–3075. doi: 10.1105/tpc.110.077974. PubMed DOI PMC
Manara A, DalCorso G, Guzzo F, Furini A. Loss of the atypical kinases ABC1K7 and ABC1K8 changes the lipid composition of the chloroplast membrane. Plant Cell Physiol. 2015;56(6):1193–1204. doi: 10.1093/pcp/pcv046. PubMed DOI
Manara A, DalCorso G, Furini A. The role of the atypical kinases ABC1K7 and ABC1K8 in abscisic acid responses. Front Plant Sci. 2016;7:366. doi: 10.3389/fpls.2016.00366. PubMed DOI PMC
Zhang Y, Behrens IV, Zimmermann R, Ludwig Y, Hey S, Hochholdinger F. LATERAL ROOT PRIMORDIA 1 of maize acts as a transcriptional activator in auxin signalling downstream of the aux/IAA gene rootless with undetectable meristem 1. J Exp Bot. 2015;66(13):3855–3863. doi: 10.1093/jxb/erv187. PubMed DOI PMC
Harris JM. Abscisic acid: hidden architect of root system structure. Plants. 2015;4(3):548–572. doi: 10.3390/plants4030548. PubMed DOI PMC
Yamaoka Y, Fujiki Y, Lee Y, Nishida I. Subcellular localization of phosphatydilserine in A. thaliana. 21st internetation conference on Arabidopsis research; 2010.
Bak G, Lee EJ, Lee Y, Kato M, Segami S, Sze H, et al. Rapid structural changes and acidification of guard cell vacuoles during stomatal closure require phosphatidylinositol 3, 5-bisphosphate. Plant Cell. 2013;25(6):2202–2216. doi: 10.1105/tpc.113.110411. PubMed DOI PMC
Perello C, Llamas E, Burlat V, Ortiz-Alcaide M, Phillips MA, Pulido P, et al. Differential subplastidial localization and turnover of enzymes involved in isoprenoid biosynthesis in chloroplasts. PLoS One. 2016;11(2):e0150539. doi: 10.1371/journal.pone.0150539. PubMed DOI PMC
Lin YC, Liu YC, Nakamura Y. The choline/ethanolamine kinase family in Arabidopsis: essential role of CEK4 in phospholipid biosynthesis and embryo development. Plant Cell. 2015;27(5):1497–1511. doi: 10.1105/tpc.15.00207. PubMed DOI PMC
Close TJ, Wanamaker SI, Caldo RA, Turner SM, Ashlock DA, Dickerson JA, et al. A new resource for cereal genomics: 22K barley GeneChip comes of age. Plant Physiol. 2004;134(3):960–968. doi: 10.1104/pp.103.034462. PubMed DOI PMC
R Core Team . R: a language and environment for statistical computing. 2015.
Gautier L, Cope L, Bolstad BM, Irizarry RA. affy---analysis of Affymetrix GeneChip data at the probe level. Bioinformatics. 2004;20(3):307–315. doi: 10.1093/bioinformatics/btg405. PubMed DOI
Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4(2):249–264. doi: 10.1093/biostatistics/4.2.249. PubMed DOI
Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mo B. 2004;3(1):1–25. doi: 10.2202/1544-6115.1027. PubMed DOI
Lucas A. Amap: another multidimensional analysis package. 2014.
Chen H. VennDiagram: generate high-resolution Venn and Euler plots. 2013.
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3(7):research0034–research0031. doi: 10.1186/gb-2002-3-7-research0034. PubMed DOI PMC
Andersen CL, Jensen JL, Ørntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 2004;64(15):5245–5250. doi: 10.1158/0008-5472.CAN-04-0496. PubMed DOI
Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper–excel-based tool using pair-wise correlations. Biotechnol Lett. 2004;26(6):509–515. doi: 10.1023/B:BILE.0000019559.84305.47. PubMed DOI
Silver N, Best S, Jiang J, Thein SL. Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Mol Biol. 2006;7(1):33. doi: 10.1186/1471-2199-7-33. PubMed DOI PMC
Prášil I, Zámečník J. The use of a conductivity measurement method for assessing freezing injury: I. Influence of leakage time, segment number, size and shape in a sample on evaluation of the degree of injury. Environ Exp Botany. 1998;40(1):1–10. doi: 10.1016/S0098-8472(98)00010-0. DOI