Physiological and transcriptional analyses of developmental stages along sugarcane leaf

BMC Plant Biology

Volumn 15, Issue 1, 2015, Pages

  Mattiello, Lucia ^a,c   Riaño Pachón, Diego Mauricio ^a   Martins, Marina Camara Mattos ^a   da Cruz, Larissa Prado ^a   Bassi, Denis ^a   Marchiori, Paulo Eduardo Ribeiro ^b   Ribeiro, Rafael Vasconcelos ^c   Labate, Mônica T Veneziano ^d   Labate, Carlos Alberto ^d   Menossi, Marcelo ^c  

^a BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^b CPqD Telecom and IT Solutions   (Brazil)

^c UNIVERSITY OF CAMPINAS   (Brazil)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Photosynthesis; RNA seq; Sugarcane

Indexed keywords

PLANT PROTEIN;

DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; PLANT LEAF; SUGARCANE;

GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; PLANT LEAVES; PLANT PROTEINS; SACCHARUM; SEQUENCE ANALYSIS, DNA;

EID: 84951951547     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-015-0694-z     Document Type: Article

References (204)

1. Tammisola J. Towards much more efficient biofuel crops - can sugarcane pave the way? GM Crops. 2010;1(4):181-98.
2. Moore P. Temporal and spatial regulation of sucrose accumulation in sugarcane stem. Aust J Plant Physiol. 1995;22(4):69-80.
3. Waclawovsky AJ, Sato PM, Lembke CG, Moore PH, Souza GM. Sugarcane for bioenergy production: an assessment of yield and regulation of sucrose content. Plant Biotechnol J. 2010;8(3):263-76.
4. D'Hont A. Unraveling the genome structure of polyploids using FISH and GISH; examples of sugarcane and banana. Cytogenet Genome Res. 2005;109(1-3):27-33.
5. D'Hont A, Grivet L, Feldmann P, Rao S, Berding N, Glaszmann JC. Characterisation of the double genome structure of modern sugarcane cultivars (Saccharum spp.) by molecular cytogenetics. Mol Gen Genet. 1996;250(4):405-13.
6. D'Hont A, Lu YH, León DG, Grivet L, Feldmann P, Lanaud C, et al. A molecular approach to unraveling the genetics of sugarcane, a complex polyploid of the Andropogoneae tribe. Genome. 1994;37(2):222-30.
7. Aitken KS, McNeil MD, Berkman PJ, Hermann S, Kilian A, Bundock PC, et al. Comparative mapping in the Poaceae family reveals translocations in the complex polyploid genome of sugarcane. BMC Plant Biol. 2014;14:190.
8. Grivet L, Arruda P. Sugarcane genomics: depicting the complex genome of an important tropical crop. Curr Opin Plant Biol. 2002;5(2):122-7.
9. Joyce P, Hermann S, O'Connell A, Dinh Q, Shumbe L, Lakshmanan P. Field performance of transgenic sugarcane produced using Agrobacterium and biolistics methods. Plant Biotech J. 2014;12(4):411-24.
10. Manickavasagam M, Ganapathi A, Anbazhagan VR, Sudhakar B, Selvaraj N, Vasudevan A, et al. Agrobacterium-mediated genetic transformation and development of herbicide-resistant sugarcane (Saccharum species hybrids) using axillary buds. Plant Cell Rep. 2004;23(3):134-43.
11. Gao SJ, Damaj MB, Park JW, Beyene G, Buenrostro-Nava MT, Molina J, et al. Enhanced transgene expression in sugarcane by co-expression of virus-encoded rna silencing suppressors. Plos One. 2013;8(6):13.
12. Molinari HBC, Marur CJ, Daros E, de Campos MKF, de Carvalho J, Bespalhok JC, et al. Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol Plant. 2007;130(2):218-29.
13. Zale J, Jung, J.H., Kim, J.Y., Pathak, B., Karan, R.Liu, H.Chen, X.Wu, H. Candreva, J.Zhai Z.Shanklin, J. Altpeter, F.: Metabolic engineering of sugarcane to accumulate energy-dense triacylglycerols in vegetative biomass. Plant Biotech J. 2015; doi: 10.1111/pbi.12411.
14. Menossi M, Silva-Filho MC, Vincentz M, Van-Sluys MA, Souza GM. Sugarcane functional genomics: gene discovery for agronomic trait development. Int J Plant Genomics. 2008;2008:458732.
15. Arruda P. Genetically modified sugarcane for bioenergy generation. Curr Opin Biotechnol. 2012;23(3):315-22.
16. Marchiori P, Machado E, Ribeiro V. Photosynthetic limitations imposed by self-shading in field-grown sugarcane varieties. Field Crops Res. 2014;155:30-7.
17. Makino A. Photosynthesis, grain yield, and nitrogen utilization in rice and wheat. Plant Physiol. 2011;155(1):125-9.
18. Long SP, Zhu XG, Naidu SL, Ort DR. Can improvement in photosynthesis increase crop yields? Plant Cell Environ. 2006;29(3):315-30.
19. 2 increases photosynthesis, biomass and productivity, and modifies gene expression in sugarcane. Plant Cell Environ. 2008;31(8):1116-27.
20. Marchiori PER, Ribeiro RV, da Silva L, Machado RS, Machado EC, Scarpari MS. Plant growth, canopy photosynthesis and light availability in three sugarcane varieties. Sugar Tech. 2010;12(2):160-6.
21. Manandhar-Shrestha K, Tamot B, Pratt EP, Saitie S, Bräutigam A, Weber AP, et al. Comparative proteomics of chloroplasts envelopes from bundle sheath and mesophyll chloroplasts reveals novel membrane proteins with a possible role in c4-related metabolite fluxes and development. Front Plant Sci. 2013;4:65.
22. 4 cycles: past, present, and future research on C4 photosynthesis. Plant Cell. 2011;23(11):3879-92.
23. 4 species. J Exp Bot. 2011;62(9):3093-102.
24. 4 photosynthesis: from evolutionary analyses to strategies for synthetic reconstruction of the trait. Curr Opin Plant Biol. 2013;16(3):315-21.
25. Wardlaw I. The control of carbon partitioning in plants. New Phytol. 1990;116(3):341-81.
26. Paul MJ, Foyer CH. Sink regulation of photosynthesis. J Exp Bot. 2001;52(360):1383-400.
27. McCormick AJ, Watt DA, Cramer MD. Supply and demand: sink regulation of sugar accumulation in sugarcane. J Exp Bot. 2009;60(2):357-64.
28. McCormick AJ, Cramer MD, Watt DA. Sink strength regulates photosynthesis in sugarcane. New Phytol. 2006;171(4):759-70.
29. Lobo AKM, Martins MD, Neto MCL, Machado EC, Ribeiro RV, Silveira JAG. Exogenous sucrose supply changes sugar metabolism and reduces photosynthesis of sugarcane through the down-regulation of Rubisco abundance and activity. J Plant Physiol. 2015;179:113-21.
30. Sheen J. Metabolic repression of transcription in higher plants. Plant Cell. 1990;2(10):1027-38.
31. Black C, Loboda T, Chen J, Sung S. Can sucrose cleavage enzymes serve as markers for sink strength and is sucrose a signal molecule during plant sink development? in International Symposium on Sucrose Metabolism. Amer Soc Plant Physiol. 1995;49-64.
32. Koch KE, Wu Y, Xu J. Sugar and metabolic regulation of genes for sucrose metabolism: potential influence of maize sucrose synthase and soluble invertase responses on carbon partitioning and sugar sensing. J Exp Bot. 1996;47 Spec No:1179-85.
33. Koch KE. Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol. 1996;47:509-40.
34. Pego JV, Kortstee AJ, Huijser C, Smeekens SC. Photosynthesis, sugars and the regulation of gene expression. J Exp Bot. 2000;51 Spec No:407-16.
35. Rolland F, Moore B, Sheen J. Sugar sensing and signaling in plants. Plant Cell. 2002;14(Suppl):S185-205.
36. Lima D, Santos H, Tiné M, Molle F, Buckeridge M. Patterns of expression of cell wall related genes in sugar cane. Genetics Mol Biol. 2001;24(1-4):191-8.
37. Carson D, Huckett B, Botha F. Sugarcane ESTs differentially expressed in immature and maturing internodal tissue. Plant Sci. 2002;162:289-300.
38. Casu RE, Jarmey JM, Bonnett GD, Manners JM. Identification of transcripts associated with cell wall metabolism and development in the stem of sugarcane by Affymetrix GeneChip Sugarcane Genome Array expression profiling. Funct Integr Genomics. 2007;7(2):153-67.
39. Casu RE, Dimmock CM, Chapman SC, Grof CP, McIntyre CL, Bonnett GD, et al. Identification of differentially expressed transcripts from maturing stem of sugarcane by in silico analysis of stem expressed sequence tags and gene expression profiling. Plant Mol Biol. 2004;54(4):503-17.
40. Casu RE, Grof CP, Rae AL, McIntyre CL, Dimmock CM, Manners JM. Identification of a novel sugar transporter homologue strongly expressed in maturing stem vascular tissues of sugarcane by expressed sequence tag and microarray analysis. Plant Mol Biol. 2003;52(2):371-86.
41. Zambrosi FCB, Ribeiro RV, Marchiori PER, Cantarella H, Landell MGA. Sugarcane performance under phosphorus deficiency: physiological responses and genotypic variation. Plant Soil. 2015;386(1-2):273-83.
42. Ribeiro RV, Machado RS, Machado EC, Machado D, Magalhaes JR, Landell MGA. Revealing drought-resistance and productive patterns in sugarcane genotypes by evaluating both physiological responses and stalk yield. Exp Agricul. 2013;49(2):212-24.
43. Cahoon AB, Takacs EM, Sharpe RM, Stern DB. Nuclear, chloroplast, and mitochondrial transcript abundance along a maize leaf developmental gradient. Plant Mol Biol. 2008;66(1-2):33-46.
44. Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, et al. The developmental dynamics of the maize leaf transcriptome. Nat Genet. 2010;42(12):1060-7.
45. Majeran W, Friso G, Ponnala L, Connolly B, Huang M, Reidel E, et al. Structural and metabolic transitions of C4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize. Plant Cell. 2010;22(11):3509-42.
46. Sharpe RM, Mahajan A, Takacs EM, Stern DB, Cahoon AB. Developmental and cell type characterization of bundle sheath and mesophyll chloroplast transcript abundance in maize. Curr Genet. 2011;57(2):89-102.
47. Chang YM, Liu WY, Shih AC, Shen MN, Lu CH, Lu MY, et al. Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis. Plant Physiol. 2012;160(1):165-77.
48. 3 photosynthesis in developing leaves of maize and rice. Nat Biotech. 2014;32:1158-65.
49. Pick TR, Bräutigam A, Schlüter U, Denton AK, Colmsee C, Scholz U, et al. Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation. Plant Cell. 2011;23(12):4208-20.
50. Silva EN, Ribeiro RV, Ferreira-Silva SL, Vieira SA, Ponte LFA, Silveira JAG. Coordinate changes in photosynthesis, sugar accumulation and antioxidative enzymes improve the performance of Jatropha curcas plants under drought stress. Biomass Bioenergy. 2012;45:270-9.
51. Ranjith SA, Meinzer FC, Perry MH, Thom M. Partitioning of carboxylase activity in nitrogen-stressed sugarcane and its relationship to bundle sheath leakiness to CO2, photosynthesis and carbon isotope discrimination. Austr J Plant Physiol. 1995;22(6):903-11.
52. Buchmann N, Brooks JR, Rapp KD, Ehleringer JR. Carbon isotope composition of C-4 grasses is influenced by light and water supply. Plant Cell Environ. 1996;19(4):392-402.
53. 2, carbon isotope discrimination, photosynthesis, and growth in sugarcane. J Exp Bot. 1996;47(300):907-14.
54. Schulze ED, Ellis R, Schulze W, Trimborn P. Diversity, metabolic types and delta C-13 carbon isotope ratios in the grass flora of Namibia in relation to growth form, precipitation and habitat conditions. Oecologia. 1996;106(3):352-69.
55. 2 concentrating system, and therefore quantum yield, in Saccharum (sugarcane) species. J Exp Bot. 1998;49(324):1227-34.
56. 2 enrichment and drought. New Phytol. 2001;150(2):285-93.
57. Cernusak LA, Ubierna N, Winter K, Holtum JA, Marshall JD GDF. Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants. New Phytol. 2013;200:950-65.
58. 4 bundle sheath leakiness at low PFD be explained by incomplete suppression of photorespiration? Plant Cell Environ. 2010;33(11):1935-48.
59. 2 uptake. Plant Physiol. 2008;148(4):2144-55.
60. 4 photosynthesis under low light conditions in Zea mays, Miscanthus x giganteus and Flaveria bidentis. Plant Cell Environ. 2013;36(2):365-81.
61. 2 isotope discrimination. J Exp Bot. 2011;62(9):3119-34.
62. Xu Z, Zhou G. Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot. 2008;59(12):3317-25.
63. Ocheltree TW, Nippert JB, Prasad PV. Changes in stomatal conductance along grass blades reflect changes in leaf structure. Plant Cell Environ. 2012;35(6):1040-9.
64. Li HL, Zhao CJ, Huang WJ, Yang GJ. Non-uniform vertical nitrogen distribution within plant canopy and its estimation by remote sensing: A review. Field Crops Res. 2013;142:75-84.
65. Valluru R, Van den Ende W. Myo-inositol and beyond - Emerging networks under stress. Plant Sci. 2011;181(4):387-400.
66. Perez-Rodriguez P, Riano-Pachon DM, Correa LGG, Rensing SA, Kersten B, Mueller-Roeber B. PInTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res. 2010;38:D822-7.
67. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139-40.
68. Ono M, Hiyama S, Higuchi Y, Kamada H, Nitasaka E, Koyama T, et al. Morphological changes in Ipomoea nil using chimeric repressors of Arabidopsis TCP3 and TCP5. Plant Biotechnol. 2012;29(5):457-63.
69. Tao Q, Guo DS, Wei BY, Zhang F, Pang CX, Jiang H, et al. The TIE1 transcriptional repressor links TCP transcription factors with TOPLESS/TOPLESS-RELATED corepressors and modulates leaf development in Arabidopsis. Plant Cell. 2013;25(2):421-37.
70. Ikeda M, Ohme-Takagi M. TCPs, WUSs, and WINDs: families of transcription factors that regulate shoot meristem formation, stem cell maintenance, and somatic cell differentiation. Front Plant Sci. 2014;5:427.
71. Aggarwal P, Padmanabhan B, Bhat A, Sarvepalli K, Sadhale PP, Nath U. The TCP4 transcription factor of Arabidopsis blocks cell division in yeast at G1 - > S transition. Biochem Biophys Res Commun. 2011;410(2):276-81.
72. Koyama T, Sato F, Ohme-Takagi M. A role of TCP1 in the longitudinal elongation of leaves in Arabidopsis. Biosci Biotechnol Biochem. 2010;74(10):2145-7.
73. Koyama T, Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M. TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell. 2010;22(11):3574-88.
74. Bischoff V, Nita S, Neumetzler L, Schindelasch D, Urbain A, Eshed R, et al. TRICHOME BIREFRINGENCE and its homolog AT5G01360 encode plant-specific DUF231 proteins required for cellulose biosynthesis in Arabidopsis. Plant Physiol. 2010;153(2):590-602.
75. Gille S, de Souza A, Xiong GY, Benz M, Cheng K, Schultink A, et al. O-Acetylation of Arabidopsis hemicellulose xyloglucan requires AXY4 or AXY4L, proteins with a TBL and DUF231 domain. Plant Cell. 2011;23(11):4041-53.
76. Gille S, Pauly M. O-acetylation of plant cell wall polysaccharides. Front Plant Sci. 2012;3:12.
77. Nielsen JS, Moller BL. Biosynthesis of cyanogenic glucosides in Triglochin maritima and the involvement of cytochrome P450 enzymes. Arch Biochem Biophys. 1999;368(1):121-30.
78. Nielsen JS, Moller BL. Cloning and expression of cytochrome P450 enzymes catalyzing the conversion of tyrosine to p-hydroxyphenylacetaldoxime in the biosynthesis of cyanogenic glucosides in Triglochin maritima. Plant Physiol. 2000;122(4):1311-21.
79. Burke JJ, Chen JP, Burow G, Mechref Y, Rosenow D, Payton P, et al. Leaf dhurrin content is a quantitative measure of the level of pre- and postflowering drought tolerance in Sorghum. Crop Sci. 2013;53(3):1056-65.
80. Curto G, Dallavalle E, De Nicola GR, Lazzeri L. Evaluation of the activity of dhurrin and sorghum towards Meloidogyne incognita. Nematology. 2012;14:759-69.
81. Busk PK, Moller BL. Dhurrin synthesis in sorghum is regulated at the transcriptional level and induced by nitrogen fertilization in older plants. Plant Physiol. 2002;129(3):1222-31.
82. Link M, Rausch T, Greiner S. In Arabidopsis thaliana, the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzyme specificities and expression profiles. Febs Letters. 2004;573(1-3):105-9.
83. Tamoi M, Tabuchi T, Demuratani M, Otori K, Tanabe N, Maruta T, et al. Point mutation of a plastidic invertase inhibits development of the photosynthetic apparatus and enhances nitrate assimilation in sugar-treated Arabidopsis seedlings. J Biol Chem. 2010;285(20):15399-407.
84. Carland F, Fujioka S, Nelson T. The sterol methyltransferases SMT1, SMT2, and SMT3 influence Arabidopsis development through nonbrassinosteroid products. Plant Physiol. 2010;153(2):741-56.
85. Giovane A, Servillo L, Balestrieri C, Raiola A, D'Avino R, Tamburrini M, et al. Pectin methylesterase inhibitor. Biochim Biophys Acta Proteins Proteomics. 2004;1696(2):245-52.
86. Davin LB, Lewis NG. Dirigent proteins and dirigent sites explain the mystery of specificity of radical precursor coupling in lignan and lignin biosynthesis. Plant Physiol. 2000;123(2):453-61.
87. Darnet S, Rahier A. Plant sterol biosynthesis: identification of two distinct families of sterol 4 alpha-methyl oxidases. Biochem J. 2004;378:889-98.
88. Bloch KE. Sterol structure and membrane-function. Crit Rev Biochem. 1983;14(1):47-92.
89. Hartmann MA. Plant sterols and the membrane environment. Trends Plant Sci. 1998;3(5):170-5.
90. Chen ZX. A superfamily of proteins with novel cysteine-rich repeats. Plant Physiol. 2001;126(2):473-6.
91. Liu ML, Li XR, Liu YB, Cao B. Regulation of flavanone 3-hydroxylase gene involved in the flavonoid biosynthesis pathway in response to UV-B radiation and drought stress in the desert plant, Reaumuria soongorica. Plant Physiol Biochem. 2013;73:161-7.
92. Winkel-Shirley B. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 2001;126(2):485-93.
93. Matkovich SJ, Zhang Y, Van Booven DJ, Dorn GW. Deep mRNA sequencing for in vivo functional analysis of cardiac transcriptional regulators application to G alpha q. Circ Res. 2010;106(9):1459-67.
94. Liu S, Lin L, Jiang P, Wang D, Xing Y. A comparison of RNA-Seq and high-density exon array for detecting differential gene expression between closely related species. Nucleic Acids Res. 2011;39(2):578-88.
95. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5(7):621-8.
96. Brautigam A, Weber APM. Do metabolite transport processes limit photosynthesis? Plant Physiol. 2011;155(1):43-8.
97. 4? Plant Cell. 2011;23(6):2087-105.
98. Kausch AP, Owen TP, Zachwieja SJ, Flynn AR, Sheen J. Mesophyll-specific, light and metabolic regulation of the C(4)PPCZm1 promoter in transgenic maize. Plant Mol Biol. 2001;45(1):1-15.
99. 3 patterns of photosynthetic gene-expression in maize. Embo J. 1988;7(12):3643-51.
100. Wingler A, Walker RP, Chen ZH, Leegood RC. Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize. Plant Physiol. 1999;120(2):539-45.
101. 4 gene expression. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:187-217.
102. 4-form phosphoenolpyruvate carboxylase with specific antibodies raised against a synthetic phosphorylated peptide. Plant J. 2000;21(1):17-26.
103. Ponnala L, Wang YP, Sun Q, van Wijk KJ. Correlation of mRNA and protein abundance in the developing maize leaf. Plant J. 2014;78(3):424-40.
104. 4 pathway genes in mesophyll and bundle sheath-cells of greening maize leaves. J Biol Chemis. 1987;262(24):11726-30.
105. Langdale JA, Rothermel BA, Nelson T. Cellular-pattern of photosynthetic gene-expression in developing maize leaves. Genes Dev. 1988;2(1):106-15.
106. Rius SP, Casati P, Iglesias AA, Gomez-Casati DF. Characterization of an Arabidopsis thaliana mutant lacking a cytosolic non-phosphorylating glyceraldehyde-3-phosphate dehydrogenase. Plant Mol Biol. 2006;61(6):945-57.
107. Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M. Trehalose metabolism in plants. Plant J. 2014;79(4):544-67.
108. Yadav UP, Ivakov A, Feil R, Duan GY, Walther D, Giavalisco P, et al. The sucrosetrehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J Exp Bot. 2014;65(4):1051-68.
109. Delorge I, Figueroa CM, Feil R, Lunn JE, Van Dijck P. Trehalose-6-phosphate synthase 1 is not the only active TPS in Arabidopsis thaliana. Biochem J. 2015;466:283-90.
110. Loewus FA, Murthy PPN. Myo-inositol metabolism in plants. Plant Sci. 2000;150(1):1-19.
111. Gillaspy GE. The cellular language of myo-inositol signaling. New Phytologist. 2011;192(4):823-39.
112. Stitt M, Gibon Y. Why measure enzyme activities in the era of systems biology? Trends Plant Sci. 2014;19(4):256-65.
113. Cosgrove D. Growth of the plant cell wall. Nat Rev Mol Cell Biol. 2005;6(11):850-61.
114. Sorek N, Sorek H, Kijac A, Szemenyei HJ, Bauer S, Hematy K, et al. The Arabidopsis COBRA protein facilitates cellulose crystallization at the plasma membrane. J Biol Chem. 2014;289(50):34911-20.
115. Ranathunge K, Schreiber L, Franke R. Suberin research in the genomics era-New interest for an old polymer. Plant Sci. 2011;180(3):399-413.
116. Kosma DK, Murmu J, Razeq FM, Santos P, Bourgault R, Molina I, et al. AtMYB41 activates ectopic suberin synthesis and assembly in multiple plant species and cell types. Plant J. 2014;80(2):216-29.
117. Mertz RA, Brutnell TP. Bundle sheath suberization in grass leaves: multiple barriers to characterization. J Exp Bot. 2014;65(13):3371-80.
118. 4 types in grasses. Austr J Plant Physiol. 1982;9(2):139-54.
119. 4 photosynthesis. Plant Physiol. 1995;108(1):173-81.
120. Soler M, Serra O, Molinas M, Huguet G, Fluch S, Figueras M. A genomic approach to suberin biosynthesis and cork differentiation. Plant Physiol. 2007;144(1):419-31.
121. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. MYB transcription factors in Arabidopsis. Trends Plant Sci. 2010;15(10):573-81.
122. Zhong RQ, Ye ZH. Complexity of the transcriptional network controlling secondary wall biosynthesis. Plant Sci. 2014;229:193-207.
123. Chai MF, Bellizzi M, Wan CX, Cui ZF, Li YB, Wang GL. The NAC transcription factor OsSWN1 regulates secondary cell wall development in Oryza sativa. J Plant Biol. 2015;58(1):44-51.
124. Ludwig Y, Berendzen KW, Xu CZ, Piepho HP, Hochholdinger F. Diversity of stability, localization, interaction and control of downstream gene activity in the maize Aux/IAA protein family. Plos One. 2014;9(9), e107346.
125. Mockaitis K, Estelle M. Auxin receptors and plant development: A new signaling paradigm. In: Annual Review of Cell and Developmental Biology, vol. 24. Palo Alto: Annual Reviews; 2008. p. 55-80.
126. Balcerowicz M, Ranjan A, Rupprecht L, Fiene G, Hoecker U. Auxin represses stomatal development in dark-grown seedlings via Aux/IAA proteins. Development. 2014;141(16):3165-76.
127. Wang YJ, Deng DX, Bian YL, Lv YP, Xie Q. Genome-wide analysis of primary auxin-responsive Aux/IAA gene family in maize (Zea mays. L.). Mol Biol Rep. 2010;37(8):3991-4001.
128. Huang CJ, Hu GJ, Li FF, Li YQ, Wu JX, Zhou XP. NbPHAN, a MYB transcriptional factor, regulates leaf development and affects drought tolerance in Nicotiana benthamiana. Physiol Plant. 2013;149(3):297-309.
129. Naz AA, Raman S, Martinez CC, Sinha NR, Schmitz G, Theres K. Trifoliate encodes an MYB transcription factor that modulates leaf and shoot architecture in tomato. Proc Natl Acad Sci U S A. 2013;110(6):2401-6.
130. Juarez MT, Twigg RW, Timmermans MCP. Specification of adaxial cell fate during maize leaf development. Development. 2004;131(18):4533-44.
131. Liu T, Ohashi-Ito K, Bergmann DC. Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses. Development. 2009;136(13):2265-76.
132. Li ZY, Li B, Dong AW. The Arabidopsis transcription factor AtTCP15 regulates endoreduplication by modulating expression of key cell-cycle genes. Mol Plant. 2012;5(1):270-80.
133. Kieffer M, Master V, Waites R, Davies B. TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis. Plant J. 2011;68(1):147-58.
134. Steiner E, Efroni I, Gopalraj M, Saathoff K, Tseng TS, Kieffer M, et al. The Arabidopsis o-linked n-acetylglucosamine transferase SPINDLY interacts with class I TCPs to Facilitate cytokinin responses in leaves and flowers. Plant Cell. 2012;24(1):96-108.
135. Uberti-Manassero NG, Lucero LE, Viola IL, Vegetti AC, Gonzalez DH. The class I protein AtTCP15 modulates plant development through a pathway that overlaps with the one affected by CIN-like TCP proteins. J Exp Bot. 2012;63(2):809-23.
136. Balazadeh S, Riano-Pachon DM, Mueller-Roeber B. Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol. 2008;10:63-75.
137. Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, et al. Arabidopsis transcription factors: Genome-wide comparative analysis among eukaryotes. Science. 2000;290(5499):2105-10.
138. Xu XP, Chen CH, Fan BF, Chen ZX. Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell. 2006;18(5):1310-26.
139. Fang YJ, You J, Xie KB, Xie WB, Xiong LZ. Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genomics. 2008;280(6):547-63.
140. Okamoto M, Vidmar JJ, Glass ADM. Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: Responses to nitrate provision. Plant Cell Physiol. 2003;44(3):304-17.
141. Robinson SA, Slade AP, Fox GG, Phillips R, Ratcliffe RG, Stewart GR. The role of glutamate-dehydrogenase in plant nitrogen-metabolism. Plant Physiol. 1991;95(2):509-16.
142. Tamura W, Hidaka Y, Tabuchi M, Kojima S, Hayakawa T, Sato T, et al. Reverse genetics approach to characterize a function of NADH-glutamate synthase1 in rice plants. Amino Acids. 2010;39(4):1003-12.
143. Prinsi B, Espen L. Mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize. BMC Plant Biol. 2015;15:13.
144. Sechley KA, Yamaya T, Oaks A. Compartmentation of nitrogen assimilation in higher-plants. Int Rev Cytol. 1992;134:85-163.
145. Feild TS, Lee DW, Holbrook NM. Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood. Plant Physiol. 2001;127(2):566-74.
146. Gepstein S. Leaf senescence - not just a 'wear and tear' phenomenon. Genome Biol. 2004;5:212.
147. Guo YF, Gan SS. Leaf senescence: Signals, execution, and regulation. Curr Top Dev Biol. 2005;71:83-112.
148. Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, et al. Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotech J. 2008;6(5):486-503.
149. Vangysel A, Vanmontagu M, Inze D. A negatively light-regulated gene from Arabidopsis thaliana encodes a protein showing high similarity to blue copper-binding proteins. Gene. 1993;136(1-2):79-85.
150. Stone SL, Hauksdottir H, Troy A, Herschleb J, Kraft E, Callis J. Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol. 2005;137(1):13-30.
151. Miao Y, Zentgraf U. A HECT E3 ubiquitin ligase negatively regulates Arabidopsis leaf senescence through degradation of the transcription factor WRKY53. Plant J. 2010;63(2):179-88.
152. Berghold J, Breuker K, Oberhuber M, Hortensteiner S, Krautler B. Chlorophyll breakdown in spinach: on the structure of five nonfluorescent chlorophyll catabolites. Photosynth Res. 2002;74(2):109-19.
153. Hortensteiner S. Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci. 2009;14(3):155-62.
154. Park SY, Yu JW, Park JS, Li J, Yoo SC, Lee NY, et al. The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell. 2007;19(5):1649-64.
155. Neill SJ, Burnett EC, Desikan R, Hancock JT. Cloning of a wilt-responsive cDNA from an Arabidopsis thaliana suspension culture cDNA library that encodes a putative 9-cis-epoxy-carotenoid dioxygenase. J Exp Bot. 1998;49(328):1893-4.
156. Barry C, Fox E, Yen H, Lee S, Ying T, Grierson D, et al. Analysis of the ethylene response in the epinastic mutant of tomato. Plant Physiol. 2001;127(1):58-66.
157. Kim J, Chang C, Tucker ML. To grow old: regulatory role of ethylene and jasmonic acid in senescence. Front Plant Sci. 2015;6:20.
158. Picton S, Barton SL, Bouzayen M, Hamilton AJ, Grierson D. Altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene-forming enzyme transgene. Plant J. 1993;3(3):469-81.
159. Grbic V, Bleecker AB. Ethylene regulates the timing of leaf senescence in Arabidopsis. Plant J. 1995;8(4):595-602.
160. John I, Drake R, Farrell A, Cooper W, Lee P, Horton P, et al. Delayed leaf senescence in ethylene-deficient ACC-oxidase antisense tomato plants - Molecular and physiological analysis. Plant J. 1995;7(3):483-90.
161. Yang TF, Gonzalez-Carranza ZH, Maunders MJ, Roberts JA. Ethylene and the regulation of senescence processes in transgenic Nicotiana sylvestris plants. Ann Bot. 2008;101(2):301-10.
162. Hochheiser H, Shneiderman B. Dynamic query tools for time series data sets, Timebox widgets for interactive exploration. Inf Vis. 2004;3(1):1-18.
163. Sade N, Shatil-Cohen A, Attia Z, Maurel C, Boursiac Y, Kelly G, et al. The role of plasma membrane aquaporins in regulating the bundle sheath-mesophyll continuum and leaf hydraulics. Plant Physiol. 2014;166(3):1609-20.
164. Franken P, Schrell S, Peterson PA, Saedler H, Wienand U. Molecular analysis of protein domain function encoded by the myb-homologous maize gene-C1, gene-ZM-1 and gene-ZM-38. Plant J. 1994;6(1):21-30.
165. Glover BJ, Perez-Rodriguez M, Martin C. Development of several epidermal cell types can be specified by the same MYB-related plant transcription factor. Development. 1998;125(17):3497-508.
166. Lee MM, Schiefelbein J. WEREWOLF, a MYB-related protein in arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell. 1999;99(5):473-83.
167. Vaucheret H. Plant ARGONAUTES. Trends Plant Sci. 2008;13(7):350-8.
168. Ferreira TH, Gentile A, Vilela RD, Costa GGL, Dias LI, Endres L, et al. microRNAs associated with drought response in the bioenergy crop sugarcane (Saccharum spp.). Plos One. 2012;7(10):14.
169. Gentile A, Ferreira TH, Mattos RS, Dias LI, Hoshino AA, Carneiro MS, et al. Effects of drought on the microtranscriptome of field-grown sugarcane plants. Planta. 2013;237(3):783-98.
170. Bottino MC, Rosario S, Grativol C, Thiebaut F, Rojas CA, Farrineli L, et al. High-throughput sequencing of small rna transcriptome reveals salt stress regulated microRNAs in Sugarcane. Plos One. 2013;8(3):12.
171. Nonomura KI, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika H, et al. A germ cell-specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell. 2007;19(8):2583-94.
172. Olmedo-Monfil V, Duran-Figueroa N, Arteaga-Vazquez M, Demesa-Arevalo E, Autran D, Grimanelli D, et al. Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature. 2010;464:628-32.
173. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 1998;17(1):170-80.
174. Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P, et al. The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development. 1999;126(3):469-81.
175. Moussian B, Schoof H, Haecker A, Jurgens G, Laux T. Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J. 1998;17(6):1799-809.
176. Yang KZ, Jiang M, Le J. A new loss-of-function allele 28y reveals a role of ARGONAUTE1 in limiting asymmetric division of stomatal lineage ground cell. J Integr Plant Biol. 2014;56(6):539-49.
177. Oliver C, Santos JL, Pradillo M. On the role of some ARGONAUTE proteins in meiosis and DNA repair in Arabidopsis thaliana. Front Plant Sci. 2014;5:177.
178. Nagasaki H, Itoh JI, Hayashi K, Hibara KI, Satoh-Nagasawa N, Nosaka M, et al. The small interfering RNA production pathway is required for shoot meristern initiation in rice. Proc Natl Acad Sci U S A. 2007;104(37):14867-71.
179. Kalve S, De Vos D, Beemster GTS. Leaf development: a cellular perspective. Front Plant Sci. 2014;5:362.
180. Jia XL, Li MY, Jiang Q, Xu ZS, Wang F, Xiong AS. High-throughput sequencing of small RNAs and anatomical characteristics associated with leaf development in celery. Sci Rep. 2015; 5: doi: 10.1038/srep11093.
181. Lakhotia N, Joshi G, Bhardwaj AR, Katiyar-Agarwal S, Agarwal M, Jagannath A, et al. Identification and characterization of miRNAome in root, stem, leaf and tuber developmental stages of potato (Solanum tuberosum L.) by high-throughput sequencing. BMC Plant Biol. 2014;14.
182. van Dillewijn C. Botany of Sugarcane. Waltahm, Massachusetts: Chronica Botanica; 1952.
183. Gibon Y, Blaesing OE, Hannemann J, Carillo P, Hohne M, Hendriks JHM, et al. A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: Comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell. 2004;16(12):3304-25.
184. 4 photosynthesis. In: Methods in Plant Biochemistry. Edited by Lea P, vol. 3. London, UK: Academic Press; 1990: 39-71.
185. Lilley RM, Walker DA. Improved spectrophotometric assay for ribulose-bis-phosphate carboxylase. Biochim Biophys Acta. 1974;358(1):226-9.
186. Carmo-Silva AE, Salvucci ME. The regulatory properties of Rubisco activase differ among species and affect photosynthetic induction during light transitions. Plant Physiol. 2013;161(4):1645-55.
187. Berkelman T, Stenstedt T: 2-D eletrophoresis-using immobilized pH gradients. Principles and Methods.: Amersham Biosciences; 1998.
188. 4 species. Austr J Plant Physiol. 1983;10(2):205-26.
189. Cross JM, von Korff M, Altmann T, Bartzetko L, Sulpice R, Gibon Y, et al. Variation of enzyme activities and metabolite levels in 24 Arabidopsis accessions growing in carbon-limited conditions. Plant Physiol. 2006;142(4):1574-88.
190. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, et al. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 2009;37(6), e45.
191. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114-20.
192. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotech. 2011;29:644-52.
193. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8(8):1494-512.
194. Smith-Unna D, Boursnell C, Kelly S, Hibberd J. Transrate v1.0.0alpha. 2014. 10.5281/zenodo.12286.
195. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, et al. The Sorghum bicolor genome and the diversification of grasses. Nature. 2009;457:551-6.
196. Parra G, Bradnam K, Korf I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genornes. Bioinformatics. 2007;23(9):1061-7.
197. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8(10):785-6.
198. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol. 2001;305(3):567-80.
199. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007;35(9):3100-8.
200. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007;35:W182-5.
201. Goodstein DM, Shu SQ, Howson R, Neupane R, Hayes RD, Fazo J, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40(D1):D1178-86.
202. Roberts A, Pachter L. Streaming fragment assignment for real-time analysis of sequencing experiments. Nat Methods. 2013;10:71-3.
203. Anders S, McCarthy DJ, Chen YS, Okoniewski M, Smyth GK, Huber W, et al. Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nature Protoc. 2013;8(9):1765-86.
204. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010; 11: doi: 10.1186/gb-2010-11-3-r25.