Boechera species exhibit species-specific responses to combined heat and high light stress

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Gallas, Genna ^a   Waters, Elizabeth R ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPHYLL; ARABIDOPSIS PROTEIN; PLANT PROTEIN;

ARTICLE; ASCORBATE PEROXIDASE 2 GENE; BOECHERA; BRASSICACEAE; CHLOROSIS; CONTROLLED STUDY; FLUORESCENCE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HEAT SHOCK TRANSCRIPTION FACTOR A2 GENE; HEAT STRESS; HEAT TOLERANCE; LEAF DAMAGE; LIGHT STRESS; MARKER GENE; NONHUMAN; PLANT GENE; PLANT RESPONSE; SPECIES DIFFERENCE; ARABIDOPSIS; CHEMISTRY; CLASSIFICATION; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT; HEAT SHOCK RESPONSE; LIGHT; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF;

ARABIDOPSIS THALIANA; BOECHERA; BRASSICACEAE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSICACEAE; CHLOROPHYLL; FLUORESCENCE; GENE EXPRESSION REGULATION, PLANT; HEAT-SHOCK RESPONSE; HOT TEMPERATURE; LIGHT; PLANT LEAVES; PLANT PROTEINS; SPECIES SPECIFICITY; STRESS, PHYSIOLOGICAL;

EID: 84932625234     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0129041     Document Type: Article

References (62)

1. Windham MD, Al-Shehbaz IA (2006) New and noteworthy species of Boechera (Brassicaceae) I: Sexual diploids. Harvard Papers in Botany 11: 61-88.
2. Windham MD, Al-Shehbaz IA (2007) New and noteworthy species of Boechera (Brassicaceae) II: Apomictic hybrids. Harvard Papers in Botany 11: 257-274.
3. Windham MD, Al-Shehbaz IA (2007) New and noteworthy species of Boechera (Brassicaceae) III: Additional sexual diploids and apomictic hybrids. Harvard Papers in Botany 12: 235-257.
4. Franzke A, Lysak MA, Al-Shehbaz IA, Koch MA, Mummenhoff K (2011) Cabbage family affairs: the evolutionary history of Brassicaceae. Trends in Plant Science 16: 108-116. doi: 10.1016/j.tplants. 2010.11.005 PMID: 21177137
5. Alexander PJ, Windham MD, Beck JB, Al-Shehbaz IA, Allphin L, et al. (2013) Molecular Phylogenetics and Taxonomy of the Genus Boechera and Related Genera (Brassicaceae: Boechereae). Systematic Botany 38: 192-209.
6. Vierling E (1991) The heat shock response in plants. Ann Rev Plant Physiol Plant Mol Biol 42: 579-620.
7. Kotak S, Larkindale J, Lee U, von Koskull-Doering P, Vierling E, et al. (2007) Complexity of the heat stress response in plants. Current Opinion in Plant Biology 10: 310-316. PMID: 17482504
8. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Roles of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Sci 9: 244-252. PMID: 15130550
9. Robinson SA (2001) Plant Light Stress. eLS: John Wiley & Sons, Ltd.
10. Franklin KA, Toledo-Ortiz G, Pyott DE, Halliday KJ (2014) Interaction of light and temperature signalling. Journal of Experimental Botany 65: 2859-2871. doi: 10.1093/jxb/eru059 PMID: 24569036.
11. Johnson SM, Lim F-L, Finkler A, Fromm H, Slabas AR, et al. (2014) Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress. Bmc Genomics 15.
12. Jung H-S, Crisp PA, Estavillo GM, Cole B, Hong F, et al. (2013) Subset of heat-shock transcription factors required for the early response of Arabidopsis to excess light. Proceedings of the National Academy of Sciences of the United States of America 110: 14474-14479. doi: 10.1073/pnas.1311632110 PMID: 23918368.
13. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. Journal of Experimental Botany 63: 1593-1608. doi: 10.1093/jxb/err460 PMID: 22291134.
14. Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. Journal of Experimental Botany 63: 3523-3543. doi: 10.1093/jxb/ers100 PMID: 22467407.
15. Rizhsky L, Liang HJ, Shuman J, Shulaev V, Davletova S, et al. (2004) When Defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology 134: 1683-1696. PMID: 15047901.
16. Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, et al. (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell and Environment 37: 1059-1073. doi: 10.1111/pce.12199 PMID: 24028172.
17. Mittler R, Blumwald E (2010) Genetic Engineering for Modern Agriculture: Challenges and Perspectives. Annual Review of Plant Biology, Vol 61 61: 443-462. doi: 10.1146/annurev-arplant-042809- 112116 PMID: 20192746.
18. Baker NR (2008) Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annual Review of Plant Biology 59: 89-113. doi: 10.1146/annurev.arplant.59.032607.092759 PMID: 18444897.
19. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. Journal of Experimental Botany 51: 659-668. PMID: 10938857.
20. Rohácek K, Soukupová J, Barták M (2008) Chlorophyll fluorescence: A wonderful tool to study plant physiology and plant stress. In: Schoefs B, editor. Schoefs B (ed) Plant Cell Compartments-Selected Topics. Kerala, India: Research Signpost. pp. pp. 41-104.
21. Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiology 130: 1109-1120. PMID: 12427978.
22. Panchuk II, Volkov RA, Schoffl F (2002) Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiology 129: 838-853. PMID: 12068123.
23. Schramm F, Ganguli A, Kiehlmann E, Englich G, Walch D, et al. (2006) The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Molecular Biology 60: 759-772. PMID: 16649111.
24. Adamska I (1997) ELIPs-Light-induced stress proteins. Physiologia Plantarum 100: 794-805.
25. Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, et al. (2003) Early light-induced proteins protect arabidopsis from photooxidative stress. Proceedings of the National Academy of Sciences of the United States of America 100: 4921-4926. PMID: 12676998.
26. von Koskull-Doering P, Scharf K-D, Nover L (2007) The diversity of plant heat stress transcription factors. Trends in Plant Science 12: 452-457. PMID: 17826296.
27. Scharf K-D, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: Structure, function and evolution. Biochimica Et Biophysica Acta-Gene Regulatory Mechanisms 1819: 104-119. doi: 10.1016/j.bbagrm.2011.10.002 PMID: 22033015.
28. Yeh C-H, Kaplinsky NJ, Hu C, Charng Y-Y (2012) Some like it hot, some like it warm: Phenotyping to explore thermotolerance diversity. Plant Science 195: 10-23. doi: 10.1016/j.plantsci.2012.06.004 PMID: 22920995.
29. Walz HWG (2007) Junior-PAM Teaching Chlorophyll Fluorometer Operator's Guide. Germany: Heinz Walz GmbH.
30. Vollenweider P, Gunthardt-Goerg MS (2006) Diagnosis of abiotic and biotic stress factors using the visible symptoms in foliage. Environmental pollution (Barking, Essex: 1987) 140: 562-571. PMID: 16602147.
31. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, et al. (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Advances in bioinformatics 2008: 420747-420747. doi: 10.1155/2008/420747 PMID: 19956698.
32. Hruz T, Wyss M, Docquier M, Pfaffl MW, Masanetz S, et al. (2011) RefGenes: identification of reliable and condition specific reference genes for RT-qPCR data normalization. Bmc Genomics 12.
33. Yuan JS, Wang D, Stewart CN Jr. (2008) Statistical methods for efficiency adjusted real-time PCR quantification. Biotechnology Journal 3: 112-123. PMID: 18074404.
34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: 402-408. PMID: 11846609.
35. Software C (2007) SYSTAT. In: Systat Software asoCSIL, editor. 12.0 ed.
36. Caverzan A, Bonifacio A, Carvalho FEL, Andrade CMB, Passaia G, et al. (2014) The knockdown of chloroplastic ascorbate peroxidases reveals its regulatory role in the photosynthesis and protection under photo-oxidative stress in rice. Plant Science 214: 74-87. doi: 10.1016/j.plantsci.2013.10.001 PMID: 24268165.
37. Larkindale J, Vierling E (2008) Core genome responses involved in acclimation to high temperature. Plant Physiol 146: 748-761. PMID: 18055584.
38. Frank G, Pressman E, Ophir R, Althan L, Shaked R, et al. (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. Journal of Experimental Botany 60: 3891-3908. doi: 10.1093/jxb/erp234 PMID: 19628571.
39. Wang X, Cai J, Jiang D, Liu F, Dai T, et al. (2011) Pre-anthesis high-temperature acclimation alleviates damage to the flag leaf caused by post-anthesis heat stress in wheat. J Plant Physiol 168: 585-593. doi: 10.1016/j.jplph.2010.09.016 PMID: 21247658.
40. Amano M, Iida S, Kosuge K (2012) Comparative studies of thermotolerance: different modes of heat acclimation between tolerant and intolerant aquatic plants of the genus Potamogeton. Annals of Botany 109: 443-452. doi: 10.1093/aob/mcr300 PMID: 22147547.
41. Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and Responding to Excess Light. Annual Review of Plant Biology 60: 239-260. doi: 10.1146/annurev.arplant.58.032806.103844 PMID: 19575582.
42. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochimica Et Biophysica Acta-Bioenergetics 1767: 414-421.
43. Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends in Plant Science 13: 178-182. doi: 10.1016/j.tplants.2008.01.005 PMID: 18328775.
44. Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends in Plant Science 16: 53-60. doi: 10.1016/j.tplants.2010.10.001 PMID: 21050798.
45. Kangasjarvi S, Neukermans J, Li S, Aro E-M, Noctor G (2012) Photosynthesis, photorespiration, and light signalling in defence responses. Journal of Experimental Botany 63: 1619-1636. doi: 10.1093/jxb/err402 PMID: 22282535.
46. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochimica Et Biophysica Acta-Bioenergetics 1757: 742-749. PMID: 16784721.
47. Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Annals of Botany 106: 1-16. doi: 10.1093/aob/mcq059 PMID: 20338950.
48. Nath K, Jajoo A, Poudyal RS, Timilsina R, Park YS, et al. (2013) Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions. Febs Letters 587: 3372-3381. doi: 10.1016/j.febslet.2013.09.015 PMID: 24056074.
49. Jaspers P, Kangasjarvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiologia Plantarum 138: 405-413. doi: 10.1111/j.1399-3054.2009.01321.x PMID: 20028478.
50. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell and Environment 35: 259-270. doi: 10.1111/j.1365-3040.2011.02336.x PMID: 21486305.
51. Kulheim C, Agren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297: 91-93. PMID: 12098696.
52. Tzvetkova-Chevolleau T, Franck F, Alawady AE, Dall'Osto L, Carriere F, et al. (2007) The light stressinduced protein ELIP2 is a regulator of chlorophyll synthesis in Arabidopsis thaliana. Plant Journal 50: 795-809. PMID: 17553115.
53. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, et al. (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284: 654-657. PMID: 10213690.
54. Rossel JB, Walter PB, Hendrickson L, Chow WS, Poole A, et al. (2006) A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. Plant Cell and Environment 29: 269-281. PMID: 17080642.
55. Somero G (2005) Linking biogeography to physiology: Evolutionary and acclimatory adjustments of thermal limits. Frontiers in Zoology 2: 1-9. PMID: 15679952.
56. Song BH, Clauss MJ, Pepper A, Mitchell-Olds T (2006) Geographic patterns of microsatellite variation in Boechera stricta, a close relative of Arabidopsis. Molecular Ecology 15: 357-369. PMID: 16448406.
57. Kiefer C, Koch MA (2012) A Continental-Wide Perspective: The Genepool of Nuclear Encoded Ribosomal DNA and Single-Copy Gene Sequences in North American Boechera (Brassicaceae). Plos One 7.
58. Stitt M (2014) Chill out with rockcress: quantitative genetics of frost tolerance in the North American wild perennial Boechera stricta. Plant, Cell & Environment 37: 2453-2455.
59. Rushworth CA, Song B-H, Lee C-R, Mitchell-Olds T (2011) Boechera, a model system for ecological genomics. Molecular ecology 20: 4843-4857. doi: 10.1111/j.1365-294X.2011.05340.x PMID: 22059452.
60. Rabeler RK (1993) THE JEPSON MANUAL-HIGHER-PLANTS OF CALIFORNIA-HICKMAN,JC. Science 262: 261-261. PMID: 17841875.
61. Comai L (2005) The advantages and disadvantages of being polyploid. Nature Reviews Genetics 6: 836-846. PMID: 16304599.
62. Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine 'winners' and 'losers'. Journal of Experimental Biology 213: 912-920. doi: 10. 1242/jeb.037473 PMID: 20190116