Fertility in barley flowers depends on Jekyll functions in male and female sporophytes

New Phytologist

Volumn 194, Issue 1, 2012, Pages 142-157

  Radchuk, Volodymyr ^a   Kumlehn, Jochen ^a   Rutten, Twan ^a   Sreenivasulu, Nese ^a   Radchuk, Ruslana ^a   Rolletschek, Hardy ^a   Herrfurth, Cornelia ^b   Feussner, Ivo ^b   Borisjuk, Ljudmilla ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Cereals; Fertility; Flower; Gametophyte sporophyte interactions; Gene expression; Sexual reproduction

Indexed keywords

CARBON; CYCLOPENTANE DERIVATIVE; JASMONIC ACID; MESSENGER RNA; OXYLIPIN; VEGETABLE PROTEIN;

ADAPTATION; BARLEY; FEMALE; FERTILITY; FERTILIZATION (REPRODUCTION); FLOWER; FLOWERING; GAMETOPHYTE; GENE EXPRESSION; HORMONE; MALE; MEMBRANE; PHENOTYPIC PLASTICITY; POLLEN; SPOROPHYTE; TRANSGENIC PLANT;

ARTICLE; CYTOLOGY; DOWN REGULATION; FERTILITY; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HORDEUM; INTRACELLULAR MEMBRANE; METABOLISM; PLANT SEED; PROTEIN TRANSPORT; RNA TRANSPORT; TRANSGENIC PLANT; ULTRASTRUCTURE; UPREGULATION;

CARBON; CYCLOPENTANES; DOWN-REGULATION; FERTILITY; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GERM CELLS, PLANT; HORDEUM; INTRACELLULAR MEMBRANES; OXYLIPINS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTEIN TRANSPORT; RNA TRANSPORT; RNA, MESSENGER; SEEDS; UP-REGULATION;

HORDEUM; HORDEUM VULGARE;

EID: 84857452533     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2011.04032.x     Document Type: Article

References (84)

1. Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S. 2005. The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES 1 and 2 control male sporogenesis. Plant Cell 17: 3337-3349.
2. Beals TP, Goldberg RB. 1997. A novel cell ablation strategy blocks tobacco anther dehiscence. Plant Cell 9: 1527-1545.
3. Blackmore S, Wortley AH, Skvarla JJ, Rowley JR. 2007. Pollen wall development in flowering plants. New Phytologist 174: 483-498.
4. Bolstad BM, Irizarry RA, Astrand M, Speed TP. 2003. A comparison of normalization methods for high density oligonucleotide array data based on bias and variance. Bioinformatics 19: 185-193.
5. Borg M, Brownfield L, Twell D. 2009. Male gametophyte development: a molecular perspective. Journal of Experimental Botany 60: 1465-1478.
6. Bosch M, Franklin-Tong VE. 2008. Self-incompatibility in Papaver: signalling to trigger PCD in incompatible pollen. Journal of Experimental Botany 59: 481-490.
7. Brambilla V, Kater M, Colombo L. 2008. Ovule integument identity determination in Arabidopsis. Plant Signaling and Behavior 3: 246-247.
8. Brownfield L, Hafidh S, Durbarry A, Khatab H, Sidorova A, Doerner P, Twell D. 2009. Arabidopsis DUO POLLEN3 is a key regulator of male germline development and embryogenesis. Plant Cell 21: 1940-1956.
9. Cacas J. 2010. Devil inside: does plant programmed cell death involve the endomembrane system? Plant, Cell & Environment 33: 1453-1473.
10. Canales C, Bhatt AM, Scott R, Dickinson H. 2002. EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Current Biology 12: 1718-1727.
11. Cecchetti V, Altamura MM, Falasca G, Costantino P, Cardarelli M. 2008. Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20: 1760-1774.
12. Chang F, Wang Y, Wang S, Ma H. 2011. Molecular control of microsporogenesis in Arabidopsis. Current Opinion in Plant Biology 14: 66-73.
13. Coffeen WC, Wolpert TJ. 2004. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 16: 857-873.
14. Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI. 2005. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES 1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17: 3350-3361.
15. Cosgrove DJ. 2005. Growth of the plant cell wall. Nature Reviews Molecular Cell Biology 6: 850-861.
16. Crawford BC, Yanofsky MF. 2008. The formation and function of the female reproductive tract in flowering plants. Current Biology 18: R972-R978.
17. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. 2005. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology 139: 5-17.
18. Denecke J. 2007. Endoplasmic reticulum. In: Roberts K, ed. Handbook of plant science. Hoboken, NJ, USA: Wiley, 223-227.
19. Durbarry A, Vizir I, Twell D. 2005. Male germ line development in Arabidopsis: duo pollen mutants reveal gametophytic regulators of generative cell cycle progression. Plant Physiology 137: 297-307.
20. Edlund AF, Swanson R, Preuss D. 2004. Pollen and stigma structure and function: the role of diversity in pollination. Plant Cell 16: S84-S97.
21. Ellerström M, Reidt W, Ivanov R, Tiedemann J, Melzer M, Tewes A, Moritz T, Mock HP, Sitbon F, Rask L et al. 2005. Ectopic expression of EFFECTOR OF TRANSCRIPTION perturbs gibberellin-mediated plant developmental processes. Plant Molecular Biology 59: 663-681.
22. Farmer EE. 2007. Plant biology: jasmonate perception machines. Nature 448: 659-660.
23. Feng X, Dickinson HG. 2007. Packaging the male germline in plants. Trends in Genetics 23: 503-510.
24. Feng X, Dickinson HG. 2010. Tapetal cell fate, lineage and proliferation in the Arabidopsis anther. Development 137: 2409-2416.
25. Fiebig A, Kimport R, Preuss D. 2004. Comparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification. Proceedings of the National Academy of Sciences, USA 101: 3286-3291.
26. Fuji S, Toriyama K. 2008. Genome barriers between nuclei and mitochondria exemplified by cytoplasmic male sterility. Plant and Cell Physiology 49: 1484-1494.
27. Goldberg RB, Beals TP, Sanders PM. 1993. Anther development: basic principles and practical applications. Plant Cell 5: 1217-1229.
28. Guo WJ, Ho TH. 2008. An abscisic acid-induced protein, HVA22, inhibits gibberellin-mediated programmed cell death in cereal aleurone cells. Plant Physiology 147: 1710-1722.
29. Hwang I, Robinson DG. 2009. Transport vesicle formation in plant cells. Current Opinion in Plant Biology 12: 660-669.
30. Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K. 2001. The DEFECTIVE IN ANTHER DEHISCIENCE gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13: 2191-2209.
31. Johnson-Brousseau SA, McCormick S. 2004. A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. Plant Journal 39: 761-775.
32. Kawanabe T, Ariizumi T, Kawai-Yamada M, Uchimiya H, Toriyama K. 2006. Abolition of the tapetum suicide program ruins microsporogenesis. Plant and Cell Physiology 47: 784-787.
33. León P, Sheen J. 2003. Sugar and hormone connections. Trends in Plant Science 8: 110-116.
34. Li H, Yuan Z, Vizcay-Barrena G, Yang C, Liang W, Zong J, Wilson ZA, Zhang D. 2011a. PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiology 156: 615-630.
35. Li H, Zhang D. 2010. Biosynthesis of anther cuticle and pollen exine in rice. Plant Signaling & Behavior 5: 1121-1123.
36. Li N, Zhang DS, Liu HS, Yin CS, Li X, Liang W, Yuan Z, Xu B, Chu HW, Wang J et al. 2006. The rice Tapetum Degeneration Retardation gene is required for tapetum degradation and anther development. Plant Cell 18: 2999-3014.
37. Li X, Gao X, Wei Y, Deng L, Ouyang Y, Chen G, Li X, Zhang Q, Wu C. 2011b. Rice APOPTOSIS INHIBITOR5 coupled with two DEAD-box adenosine 5'-triphosphate-dependent RNA helicases regulates tapetum degeneration. Plant Cell 23: 1416-1434.
38. -ΔΔCT method. Methods 25: 402-408.
39. Luigi B, Papini A, Milocani E, Vesprini JL. 2006. Programmed cell death in the nucellus of Tillandsia (Bromeliaceae). Caryologia 59: 334-339.
40. Luo ZB, Janz D, Jiang X, Göbel C, Wildhagen H, Tan Y, Rennenberg H, Feussner I, Polle A. 2009. Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiology 151: 1902-1917.
41. Ma H. 2005. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annual Review of Plant Biology 56: 393-434.
42. Mandaokar A, Browse J. 2009. MYB108 acts together with MYB24 to regulate jasmonate-mediated stamen maturation in Arabidopsis. Plant Physiology 149: 851-862.
43. Maraschin SF, de Priester W, Spaink HP, Wang M. 2005. Androgenic switch: an example of plant embryogenesis from the male gametophyte perspective. Journal of Experimental Botany 56: 1711-1726.
44. Mayfield JA, Fiebig A, Johnstone SE, Preuss D. 2001. Gene families from the Arabidopsis thaliana pollen coat proteome. Science 292: 2482-2485.
45. Mayfield JA, Preuss D. 2000. Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nature Cell Biology 2: 128-130.
46. 1H NMR imaging uncovers sugar allocation in the living seed. Plant Biotechnology Journal 9: 1022-1037.
47. Morrell PL, Clegg MT. 2007. Genetic evidence for a second domestication of barley (Hordeum vulgare) east of the Fertile Crescent. Proceedings of the National Academy of Sciences, USA 104: 3289-3294.
48. Murmu J, Bush MJ, DeLong C, Li S, Xu M, Khan M, Malcolmson C, Fobert PR, Zachgo S, Hepworth SR. 2010. Arabidopsis basic leucine-zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development. Plant Physiology 154: 1492-1504.
49. Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE et al. 2005. Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132: 4107-4118.
50. Parish RW, Li SF. 2010. Death of a tapetum: a programme of developmental altruism. Plant Science 178: 73-89.
51. Piffanelli P, Ros JHE, Murphy DJ. 1998. Biogenesis and function of the lipidic structures of pollen grains. Sexual Plant Reproduction 11: 65-80.
52. Radchuk V, Borisjuk L, Radchuk R, Steinbiss HH, Rolletschek H, Broeders S, Wobus U. 2006. Jekyll encodes a novel protein involved in the sexual reproduction of barley. Plant Cell 18: 1652-1666.
53. Radchuk V, Weier D, Radchuk R, Weschke W, Weber H. 2011. Development of maternal seed tissue in barley is mediated by regulated cell expansion and cell disintegration and coordinated with endosperm growth. Journal of Experimental Botany 62: 1217-1227.
54. Ramakers C, Ruijter JM, Deprez RH, Moorman AF. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 13: 62-66.
55. Rangan TS, Rangaswamy NS. 1999. Nucellus - a unique embryologic system. Phytomorphology 49: 337-376.
56. Ravanel S, Gakiere B, Job D, Douce R. 1998. The specific features of methionine biosynthesis and metabolism in plants. Proceedings of the National Academy of Sciences, USA 95: 7805-7812.
57. Rotman N, Durbarry A, Wardle A, Yang WC, Chaboud A, Faure JE, Berger F, Twell D. 2005. A novel class of MYB factors controls sperm-cell formation in plants. Current Biology 15: 244-248.
58. Rowland O, Lee R, Franke R, Schreiber L, Kunst L. 2007. The CER3 wax biosynthetic gene from Arabidopsis thaliana is allelic to WAX2/YRE/FLP1. FEBS Letters 581: 3538-3544.
59. Rutten T, Krüger C, Melzer M, Stephan UW, Hell R. 2003. Discovery of an extended bundle sheath in Ricinus communis L. and its role as a temporal storage compartment for the iron chelator nicotianamine. Planta 217: 400-406.
60. Sanders PM, Lee PY, Biesgen C, Boone JD, Beals TP, Weiler EW, Goldberg RB. 2000. The Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway. Plant Cell 12: 1041-1061.
61. Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K. 1999. Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 96: 11664-11669.
62. Schussler JR, Westgate ME. 1995. Assimilate flux determines kernel set at low water potential in maize. Crop Science 35: 1074-1080.
63. Scott RJ, Spielman M, Dickinson HG. 2004. Stamen structure and function. Plant Cell 16: S46-S60.
64. Sreenivasulu N, Radchuk V, Strickert M, Miersch O, Weschke W, Wobus U. 2006. Gene expression patterns reveal tissue-specific signaling networks controlling programmed cell death and ABA-regulated maturation in developing barley seeds. Plant Journal 47: 310-327.
65. Sreenivasulu N, Usadel B, Winter A, Radchuk V, Scholz U, Stein N, Weschke W, Strickert M, Close TJ, Stitt M et al. 2008. Barley grain maturation and germination: metabolic pathway and regulatory network commonalities and differences highlighted by new MapMan/PageMan profiling tools. Plant Physiology 146: 1738-1758.
66. Stintzi A, Browse J. 2000. The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proceedings of the National Academy of Sciences, USA 97: 10625-10630.
67. Sun Q, Zhou DX. 2008. Rice jmjC domain-containing gene JMJ706 encodes H3K9 demethylase required for floral organ development. Proceedings of the National Academy of Sciences, USA 105: 13679-13684.
68. Sundaresan V, Alandete-Saez M. 2010. Pattern formation in miniature: the female gametophyte of flowering plants. Development 137: 179-189.
69. Varnier AL, Mazeyrat-Gourbeyre F, Sangwan RS, Clément C. 2005. Programmed cell death progressively models the development of anther sporophytic tissues from the tapetum and is triggered in pollen grains during maturation. Journal of Structural Biology 152: 118-128.
70. Vizcay-Barrena G, Wilson ZA. 2006. Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant. Journal of Experimental Botany 57: 2709-2717.
71. Wang A, Xia Q, Xie W, Datla R, Selvaraj G. 2003. The classical Ubisch bodies carry a sporophytically produced structural protein (RAFTIN) that is essential for pollen development. Proceedings of the National Academy of Sciences, USA 100: 14487-14492.
72. Wasternack C. 2007. Jasmonates: an update in biosynthesis, signal transduction and action in plant stress response, growth and development. Annals of Botany 100: 681-697.
73. Watanabe M. 2008. Towards a comprehensive understanding of molecular mechanisms of sexual reproduction in higher plants. Plant and Cell Physiology 49: 1404-1406.
74. Wetzel CLR, Jensen WA. 1992. Studies of pollen maturation in cotton: the storage reserve accumulation phase. Sexual Plant Reproduction 5: 117-127.
75. Wheeler MJ, de Graaf BH, Hadjiosif N, Perry RM, Poulter NS, Osman K, Vatovec S, Harper A, Franklin FC, Franklin-Tong VE. 2009. Identification of the pollen self-incompatibility determinant in Papaver rhoeas. Nature 459: 992-995.
76. Wilson ZA, Zhang DB. 2009. From Arabidopsis to rice: pathways in pollen development. Journal of Experimental Botany 60: 1479-1492.
77. Wu HM, Cheun AY. 2000. Programmed cell death in plant reproduction. Plant Molecular Biology 44: 267-281.
78. Yang C, Xu Z, Song J, Conner K, Vizcay-Barrena G, Wilson ZA. 2007. Arabidopsis MYB26/MALE STERILE35 regulates secondary thickening in the endothecium and is essential for anther dehiscence. Plant Cell 19: 534-548.
79. Yang WC, Shi DQ, Chen YH. 2010. Female gametophyte development in flowering plants. Annual Review of Plant Biology 61: 89-108.
80. Yang WC, Ye D, Xu J, Sundaresan V. 1999. The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes and Development 13: 2108-2117.
81. Zhang D, Luo X, Zhu L. 2011. Cytological analysis and genetic control of rice anther development. Journal of Genetics and Genomics 38: 379-390.
82. Zhao X, de Palma J, Oane R, Gamuyao R, Luo M, Chaudhury A, Hervé P, Xue Q, Bennett J. 2008. OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. Plant Journal 54: 375-387.
83. Zhao DZ, Wang GF, Speal B, Ma H. 2002. The EXCESS MICROSPOROCYTES 1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes and Development 16: 2021-2031.
84. Zuo J, Niu QW, Nishizawa N, Wu Y, Kost B, Chua NH. 2000. KORRIGAN, an Arabidopsis endo-1, 4-beta-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell 12: 1137-1152.