Chilling to zero degrees disrupts pollen formation but not meiotic microtubule arrays in Triticum aestivum L.

Plant Cell and Environment

Volumn 37, Issue 12, 2014, Pages 2781-2794

  Barton, Deborah A ^a   Cantrill, Laurence C ^a   Law, Andrew M K ^a   Phillips, Collin G ^a   Sutton, Bruce G ^a   Overall, Robyn L ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cytomixis; Freezing damage; Male sterility; meiosis; Plasmolysis; Wheat

Indexed keywords

TRITICUM; TRITICUM AESTIVUM;

PLANT DNA;

AUSTRALIA; CYTOLOGY; FREEZING; GEOGRAPHY; GROWTH, DEVELOPMENT AND AGING; MEIOSIS; MEIOTIC PROPHASE I; METABOLISM; MICROTUBULE; PHYSIOLOGY; POLLEN; POLLINATION; WHEAT;

AUSTRALIA; DNA, PLANT; FREEZING; GEOGRAPHY; MEIOSIS; MEIOTIC PROPHASE I; MICROTUBULES; POLLEN; POLLINATION; TRITICUM;

EID: 84926614885     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12358     Document Type: Article

References (78)

1. Abdrakhamanova A., Wang Q.Y., Khokhlova L. & Nick P. (2003) Is microtubule disassembly a trigger for cold acclimation? Plant and Cell Physiology 44, 676-686.
2. Al-Issawi M., Rihan H.Z., El-Sarkassy N. & Fuller M.P. (2013) Frost hardiness expression and characterisation in wheat at ear emergence. Journal of Agronomy and Crop Science 199, 66-74.
3. Bellucci M., Roscini C. & Mariani A. (2003) Cytomixis in pollen mother cells of Medicago sativa L. The Journal of Heredity 94, 512-516.
4. Bennett M.D., Smith J.B. & Kemble R. (1972) The effect of temperature on meiosis and pollen development in wheat and rye. Canadian Journal of Genetics and Cytology 14, 615-624.
5. Bhat T.A., Parveen S. & Khan A.H. (2006) MMS-induced cytomixis in pollen mother cells of broad bean (Vicia faba L.). Turkish Journal of Botany 30, 273-279.
6. Bione N.C.P., Pagliarini M.S. & de Toledo J.F.F. (2000) Meiotic behavior of several Brazilian soybean varieties. Genetics and Molecular Biology 23, 623-631.
7. Botwright Acuña T., Dean G. & Riffkin P. (2011) Constraints to achieving high potential yield of wheat in a temperate, high-rainfall environment in south-eastern Australia. Crop & Pasture Science 62, 125-136.
8. Brooking I.R. (1976) Male sterility in Sorghum bicolor (L.) Moench induced by low night temperature. I Timing of the stage of sensitivity. Australian Journal of Plant Physiology 3, 589-596.
9. Dell B. (1981) Male sterility and anther wall structure in copper-deficient plants. Annals of Botany 48, 599-608.
10. Demotes-Mainard S., Doussinault G. & Meynard J.M. (1996) Abnormalities in the male developmental programme of winter wheat induced by climatic stress at meiosis. Agronomie 16, 505-515.
11. Dorion S., Lalonde S. & Saini H.S. (1996) Induction of male sterility in wheat by meiotic-stage water deficit is preceded by a decline in invertase activity and changes in carbohydrate metabolism in anthers. Plant Physiology 111, 137-145.
12. De Storme N. & Geelen D. (2013) The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant, Cell & Environment 37, 1-18.
13. De Storme N., Copenhaver G.P. & Geelen D. (2012) Production of diploid male gametes in Arabidopsis by cold-induced destabilization of postmeiotic radial microtubule arrays. Plant Physiology 160, 1808-1826.
14. DEPI (Department of Environment and Primary Industries) Victoria (2013) The effect of frost on cereal grain crops. Retrieved from http://www.depi.vic.gov.au/agriculture-and-food/grains-and-other-crops/crop-production/effect-of-frost-on-cereal-grain-crops
15. Fischer R.A. & Stockman Y.M. (1980) Kernel number per spike in wheat (Triticum aestivum L.): responses to pre-anthesis shading. Australian Journal of Plant Physiology 7, 169-180.
16. Fletcher R.J. (1976) Physiological and genetic studies of wheat characters associated with frost resistance. PhD thesis, University of Sydney, Australia.
17. Frederiks T.M., Christopher J.T., Harvey G.L., Sutherland M.W. & Borrell A.K. (2012) Current and emerging methods to identify post-head-emergence frost adaptation in wheat and barley. Journal of Experimental Botany 63, 5405-5416.
18. Fuller M.P., Fuller A.M., Kaniouras S., Christophers J. & Fredericks T. (2007) The freezing characteristics of wheat at ear emergence. European Journal of Agronomy 26, 435-441.
19. Fuller M.P., Christopher J. & Fredericks T. (2009) Low-temperature damage to wheat in head - matching perceptions with reality. In Plant Cold Hardiness: From the Laboratory to the Field (eds L. Gusta, M. Wisniewski & K. Tanino ), pp. 12-18. CAB International, Wallingford, UK.
20. Gibson L.R. & Mullen R.E. (1996) Influence of day and night temperature on soybean seed yield. Crop Science 36, 98-104.
21. Gothandam K.M., Kim E.S. & Chung Y.Y. (2007) Ultrastructural study of rice tapetum under low-temperature stress. Journal of Plant Biology 50, 396-402.
22. Hepler P.K. & Hush J.M. (1996) Behavior of microtubules in living plant cells. Plant Physiology 112, 455-461.
23. Heslop-Harrison J. (1966) Cytoplasmic connexions between angiosperm meiocytes. Annals of Botany 30, 221-230.
24. Huang L., Pant J., Dell B. & Bell R.W. (2000) Effects of boron deficiency on anther development and floret fertility in wheat (Triticum aestivum L. 'Wilgoyne'). Annals of Botany 85, 493-500.
25. Imrie B.C. (1966) Stigma receptivity in cytoplasmic male sterile wheat. Australian Journal of Experimental Agriculture and Animal Husbandry 6, 175-178.
26. Ji X., Shiran B., Wan J., Lewis D.C., Jenkins C.L.D., Condon A.G., ... Dolferus R. (2010) Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant, Cell & Environment 33, 926-942.
27. Ji X., Dong B., Shiran B., Talbot M.J., Edlington J.E., Hughes T., ... Dolferus R. (2011) Control of abscisic acid catabolism and abscisic acid homeostasis is important for reproductive stage stress tolerance in cereals. Plant Physiology 156, 647-662.
28. Kawaguchi K., Shibuya N. & Ishii T. (1996) A novel tetrasaccharide, with a structure similar to the terminal sequence of an arabinogalactan protein, accumulates in rice anthers in a stage-specific manner. The Plant Journal 9, 777-785.
29. Kosová K., Prášil I.T., Vítámvás P., Dobrev P., Motyka V., Floková K., ... Vanková R. (2012) Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. Journal of Plant Physiology 15, 567-576.
30. Kosová K., Vítámvás P., Planchon S., Renaut J., Vanková R. & Prášil I.T. (2013) Proteome analysis of cold response in spring and winter wheat (Triticum aestivum) crowns reveals similarities in stress adaptation and differences in regulatory processes between the growth habits. Journal of Proteome Research 12, 4830-4845.
31. Kravets E.A. (2013) Cytomixis and its role in the regulation of plant fertility. Russian Journal of Developmental Biology 44, 113-128.
32. Langer R.H.M. & Olugbemi L.B. (1970) A study of New Zealand wheat: IV. Effect of extreme temperature at different stages of development. New Zealand Journal of Agricultural Research 13, 878-886.
33. Lattoo S.K., Khan S., Bamotra S. & Dhar A.K. (2006) Cytomixis impairs meiosis and influences reproductive success in Chlorophytum comosum (Thunb) Jacq. - an additional strategy and possible implications. Journal of Biosciences 31, 629-637.
34. Malallah G.A. & Attia T.A. (2003) Cytomixis and its possible evolutionary role in a Kuwaiti population of Diplotaxis harra (Brassicaceae). Botanical Journal of Linnean Society 143, 169-175.
35. Mamun E.A., Alfred S., Cantrill L.C., Overall R.L. & Sutton B.G. (2006) Effects of chilling on male gametophyte development in rice. Cell Biology International 30, 583-591.
36. Mamun E.A., Cantrill L.C., Overall R.L. & Sutton B.G. (2010) Mechanism of low-temperature-induced pollen failure in rice. Cell Biology International 34, 469-476.
37. Mercado J.A., Mar Trigo M., Reid M.S., Valpuesta V. & Quesada M.A. (1997) Effects of low temperature on pepper pollen morphology and fertility: evidence of cold induced exine alterations. Journal of Horticultural Science 72, 317-326.
38. Mizuno K. (1992) Induction of cold stability of microtubules in cultured tobacco cells. Plant Physiology 100, 740-748.
39. Monroy A.F., Dryanova A., Malette B., Oren D.H., Ridha Farajalla M., Liu W., ... Gulick P.J. (2007) Regulatory gene candidates and gene expression analysis of cold acclimation in winter and spring wheat. Plant Molecular Biology 64, 409-423.
40. Mursalimov S.R., Baiborodin S.I., Sidorchuk Y.V., Shumny V.K. & Deineko E.V. (2010) Characteristics of the cytomictic channel formation in Nicotiana tabacum L. pollen mother cells. Cytology and Genetics 44, 14-18.
41. Mursalimov S.R., Sidorchuk Y.V. & Deineko E.V. (2013) New insights into cytomixis: specific cellular features and prevalence in higher plants. Planta 238, 415-423.
42. Nguyen G.N. & Sutton B.G. (2009) Water deficit reduced fertility of young microspores resulting in a decline of viable mature pollen and grain set in rice. Journal of Agronomy & Crop Science 195, 11-18.
43. Nguyen G.N., Hailstones D.L., Wilkes M. & Sutton B.G. (2010) Role of carbohydrate metabolism in drought-induced male sterility in rice anthers. Journal of Agronomy and Crop Science 196, 346-357.
44. Okamura S., Kakiuchi M., Sano A. & Kawajiri M. (1993) Loss of tubulin during cold treatment of cultured carrot cells. Physiologia Plantarum 88, 93-98.
45. Oliver S.N., Van Dongen J.T., Alfred S.C., Mamun E.A., Zhao X., Saini H.S., ... Dolferus R. (2005) Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant, Cell & Environment 28, 1534-1551.
46. Oliver S.N., Dennis E.S. & Dolferus R. (2007) ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant and Cell Physiology 48, 1319-1330.
47. Parish R.W., Phan H.A., Iacuone S. & Li S.F. (2012) Tapetal development and abiotic stress: a centre of vulnerability. Functional Plant Biology 39, 553-559.
48. Pressman E., Peet M.M. & Pharr D.M. (2002) The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in developing anthers. Annals of Botany 90, 631-636.
49. Qian C.M., Xu A. & Liang G.H. (1986) Effects of low temperatures and genotypes on pollen development in wheat. Crop Science 26, 43-46.
50. Saini H.S., Sedgley M. & Aspinall D. (1984) Developmental anatomy in wheat of male sterility induced by heat stress, water deficit or abscisic acid. Australian Journal of Plant Physiology 11, 243-253.
51. Sakiyama M. & Shibaoka H. (1990) Effects of abscisic acid on the orientation and cold stability of cortical microtubules in epicotyl cells of the dwarf pea. Protoplasma 157, 165-171.
52. Satake T. (1976) Determination of the most sensitive stage to sterile-type cool injury in rice plants. Research Bulletin of the Hokkaido National Agricultural Experimental Station 113, 1-33.
53. Sato S., Kamiyama M., Iwata T., Makita N., Furukawa H. & Ikeda H. (2006) Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon esculentum by disrupting specific physiological processes in male reproductive development. Annals of Botany 97, 731-738.
54. Shamina N.V., Dorogova N.V., Zagorskaia A.A., Deineko E.V. & Shumnyi V.K. (2000) Disruption of male meiosis in transgenic line tobacco res91. Tsitologiia 42, 1159-1164.
55. Shemesh Mayer E., Winiarczyk K., Blaszczyk L., Kosmala A., Rabinowitch H.D. & Kamenetsky R. (2013) Male gametogenesis and sterility in garlic (Allium sativum L.): barriers on the way to fertilization and seed production. Planta 237, 103-120.
56. Simon J.R. & Salmon E.D. (1990) The structure of microtubule ends during the elongation and shortening phases of dynamic instability examined by negative-stain electron microscopy. Journal of Cell Science 96, 571-582.
57. Single W.V. (1961) Studies on frost injury to wheat. I Laboratory freezing tests in relation to the behaviour of varieties in the field. Australian Journal of Agricultural Research 12, 767-782.
58. Single W.V. (1964) Studies on frost injury to wheat. II. Ice formation within the plant. Australian Journal of Agricultural Research 15, 869-875.
59. Single W.V. & Marcellos H. (1974) Studies on frost injury to wheat. IV. Freezing of ears after emergence from the leaf sheath. Australian Journal of Agricultural Research 25, 679-686.
60. Soman T.A. & Bhavanandan K.V. (1993) Temperature sensitive cytomixis in Helicanthes elastica (Desr.) Dans. (Loranthaceae). Cytologia 58, 21-26.
61. Srinivasan A., Saxena N.P. & Johansen C. (1999) Cold tolerance during early reproductive growth of chickpea (Cicer arietinum L.): genetic variation in gamete development and function. Field Crops Research 60, 209-222.
62. Stapper M.S. (2007) Crop monitoring and Zadoks growth stages for wheat. CSIRO Plant Industry, Canberra, Australia.
63. Subedi K.D., Budhathoki C.B., Subedi M. & Sthapit B.R. (1996). Overview of wheat sterility problem and research findings to date in the western hills of Nepal. In Sterility in Wheat in Subtropical Asia: Extent, Causes and Solutions. Proceedings of workshop held from 18 to 21 September, 1995 at Lumle Agricultural Research Centre, Pokhara, Nepal. (eds H.M. Rawson & K.D. Subedi) ACIAR Proceedings No. 72, pp. 119-126.
64. Subedi K.D., Floyd C.N. & Budhathoki C.B. (1998a) Cool temperature-induced sterility in spring wheat (Triticum aestivum L.) at high altitudes in Nepal: variation among cultivars in response to sowing date. Field Crops Research 55, 141-151.
65. Subedi K.D., Gregory P.J., Summerfield R.J. & Gooding M.J. (1998b) Cold temperatures and boron deficiency caused grain set failure in spring wheat (Triticum aestivum L. Field Crops Research 57, 277-288.
66. Subedi K.D., Gregory P.J., Summerfield R.J. & Gooding M.J. (2000) Pattern of grain set in boron-deficient and cold-stressed wheat (Triticum aestivum L.). Journal of Agricultural Science 134, 25-31.
67. Subedi K.D., Gooding M.J. & Gregory P.J. (2001) Cultivar variation in boron accumulation and grain set in wheat under the influence of cold temperature. The Annals of Applied Biology 138, 97-101.
68. Tang Z., Zhang L., Yang D., Zhao C. & Zheng Y. (2011) Cold stress contributes to aberrant cytokinesis during male meiosis I in a wheat thermosensitive genic male sterile line. Plant, Cell & Environment 34, 389-405.
69. Thakur P., Kumar S., Malik J.A., Berger J.D. & Nayyar H. (2010) Cold stress effects on reproductive development in grain crops: an overview. Environmental and Experimental Botany 67, 429-443.
70. Thomashow M.F. (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology 50, 571-599.
71. Tranel D., Kanpp A. & Perdomo A. (2009) Chilling effects during maize tassel development and the lack of compensational plasticity. Crop Science 49, 1852-1858.
72. Trewin D. (2006) Year Book Australia, Number 88, p. 2006. Australian Bureau of Statistics, Canberra, Australia.
73. Wallin M. & Strömberg E. (1995) Cold-stable and cold-adapted microtubules. International Review of Cytology 157, 1-31.
74. Wood A.W., Tan D.K.Y., Mamun E.A. & Sutton B.G. (2006) Sorghum can compensate for chilling-induced grain loss. Journal of Agronomy and Crop Science 192, 445-451.
75. Woodruff D.R. (1992) 'WHEATMAN' a decision support system for wheat management in subtropical Australia. Australian Journal of Agricultural Research 43, 1483-1499.
76. Woodruff D.R. & Tonks J. (1983) Relationship between time of anthesis and grain yield of wheat genotypes with differing developmental patterns. Australian Journal of Agricultural Research 34, 1-11.
77. Zhong X., Mei X., Li Y., Yoshida H., Zhao P., Wang X., ... Sun Z. (2008) Changes in frost resistance of wheat young ears with development during jointing stage. Journal of Agronomy and Crop Science 194, 343-349.
78. Zinn K.E., Tunc-Ozdemir M. & Harper J.F. (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. Journal of Experimental Botany 61, 1959-1968.