Wheat pre-anthesis development as affected by photoperiod sensitivity genes (Ppd-1) under contrasting photoperiods
Thomas I. Pérez-Gianmarco A B F , Gustavo A. Slafer A C D and Fernanda G. González B E
+ Author Affiliations
- Author Affiliations
A Department of Crop and Forest Sciences, University of Lleida, Av. Rovira Roure 191, 25198 Lleida, Spain.
B CITNOBA, CONICET-UNNOBA. Monteagudo 2772, B2700KIZ Pergamino, Buenos Aires, Argentina.
C ICREA (Catalonian Institution for Research and Advanced Studies), Spain.
D AGROTECNIO (Centre for Research in Agrotechnology), University of Lleida, Av. Rovira Roure 191, 25198 Lleida, Spain.
E EEA INTA Pergamino. Ruta 32, Km 4,5, B2700XAC Pergamino, Buenos Aires, Argentina.
F Corresponding author. Email: t.perezgianmarco@conicet.gov.ar
Functional Plant Biology 45(6) 645-657 https://doi.org/10.1071/FP17195
Submitted: 8 July 2017 Accepted: 8 December 2017 Published: 18 January 2018
Abstract
Fine tuning wheat phenology is of paramount importance for adaptation. A better understanding of how genetic constitution modulates the developmental responses during pre-anthesis phases would help to maintain or even increase yield potential as temperature increases due to climate change. The photoperiod-sensitive cultivar Paragon, and four near isogenic lines with different combinations of insensitivity alleles (Ppd-A1a, Ppd-B1a, Ppd-D1a or their triple stack) were evaluated under short (12 h) and long (16 h) photoperiods. Insensitivity alleles decreased time to anthesis and duration of the three pre-anthesis phases (vegetative, early reproductive and late reproductive), following the Ppd-D1a > Ppd-A1a > Ppd-B1a ranking of strength. Stacking them intensified the insensitivity, but had no additive effect over that of Ppd-D1a. The late reproductive phase was the most responsive, even exhibiting a qualitative response. Leaf plastochron was not affected but spikelet plastochron increased according to Ppd-1a ranking of strength. Earlier anthesis resulted from less leaves differentiated and a fine tuning effect of accelerated rate of leaf appearance. None of the alleles affected development exclusively during any particular pre-anthesis phase, which would be ideal for tailoring time to anthesis with specific partitioning of developmental time into particular phases. Other allelic variants should be further tested to this purpose.
Additional keywords: final leaf number, insensitivity alleles, ontogenesis, phenology, primordia dynamics, spikelet number.
References
Asseng S, Ewert F, Martre P, Rötter RP, Lobell DB, Cammarano D, Kimball BA, Ottman MJ, Wall GW, White JW, et al (2015) Raising temperatures reduce global wheat production. Nature Climate Change 5, 143–147.| Raising temperatures reduce global wheat production.Crossref | GoogleScholarGoogle Scholar |
Beales J, Turner A, Griffiths S, Snape JW, Laurie DA (2007) A Pseudo-Response Regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theoretical and Applied Genetics 115, 721–733.
| A Pseudo-Response Regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsFWqsL8%3D&md5=62310c09043079874bf48eee6a1f6571CAS |
Bentley AR, Turner AS, Gosman N, Leigh FJ, Maccaferri M, Dreisigacker S, Greenland A, Laurie DA (2011) Frequency of photoperiod-insensitive Ppd-A1a alleles in tetraploid, hexaploid and synthetic hexaploid wheat germplasm. Plant Breeding 130, 10–15.
| Frequency of photoperiod-insensitive Ppd-A1a alleles in tetraploid, hexaploid and synthetic hexaploid wheat germplasm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjt1WrsbY%3D&md5=1cbc480ebad03ee6f798fd11844659a8CAS |
Bentley AR, Horsnell R, Werner CP, Turner AS, Rose GA, Bedard C, Howell P, Whilhelm EP, Mackay IJ, Howells RM, Greenland A, Laurie DA, Gosman N (2013) Short, natural, and extended photoperiod response in BC2F4 lines of bread wheat with different Photoperiod-1 (Ppd-1) alleles. Journal of Experimental Botany 64, 1783–1793.
| Short, natural, and extended photoperiod response in BC2F4 lines of bread wheat with different Photoperiod-1 (Ppd-1) alleles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmslSlu74%3D&md5=cc83c056046c88b7028ee93fb3924fdaCAS |
Cockram J, Jones H, Leigh FJ, O’Sullivan D, Powell W, Laurie DA, Greenland AJ (2007) Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity. Journal of Experimental Botany 58, 1231–1244.
| Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvFGisr4%3D&md5=75d332538b86109712a8f93990ecc607CAS |
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2015) Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. Available at http://www.infostat.com.ar [Verified 13 December 2017].
Díaz A, Zikhali M, Turner AS, Isaac P, Laurie DA (2012) Copy number variation affecting the Photoperiod-B1 and Vernalization-A1 genes is associated with altered flowering time in wheat (Triticum aestivum). PLoS One 7, e33234
| Copy number variation affecting the Photoperiod-B1 and Vernalization-A1 genes is associated with altered flowering time in wheat (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar |
Evans LT (1978) The influence of irradiance before and after anthesis on grain yield and its components in microcrops of wheat grown in a constant daylength and temperature regime. Field Crops Research 1, 5–19.
| The influence of irradiance before and after anthesis on grain yield and its components in microcrops of wheat grown in a constant daylength and temperature regime.Crossref | GoogleScholarGoogle Scholar |
Evans LT, Blundell C (1994) Some aspects of photoperiodism in wheat and its wild relatives. Australian Journal of Plant Physiology 21, 551–562.
| Some aspects of photoperiodism in wheat and its wild relatives.Crossref | GoogleScholarGoogle Scholar |
Fischer RA (1975) Yield potential in a dwarf spring wheat and the effect of shading. Crop Science 15, 607–613.
| Yield potential in a dwarf spring wheat and the effect of shading.Crossref | GoogleScholarGoogle Scholar |
Foulkes J, Sylvester-Bradley R, Worland AJ, Snape JW (2004) Effects of a photoperiod-response gene Ppd-D1 on yield potential and drought resistance in UK winter wheat. Euphytica 135, 63–73.
| Effects of a photoperiod-response gene Ppd-D1 on yield potential and drought resistance in UK winter wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvFehsLk%3D&md5=e0a547363bfcf9614157107fd2f53fc5CAS |
García GA, Dreccer MF, Miralles DJ, Serrago RA (2015) High night temperatures during grain number determination reduce wheat and barley grain yield: a field study. Global Change Biology 21, 4153–4164.
| High night temperatures during grain number determination reduce wheat and barley grain yield: a field study.Crossref | GoogleScholarGoogle Scholar |
González FG, Slafer GA, Miralles DJ (2002) Vernalization and photoperiod responses in wheat pre-flowering reproductive phases. Field Crops Research 74, 183–195.
| Vernalization and photoperiod responses in wheat pre-flowering reproductive phases.Crossref | GoogleScholarGoogle Scholar |
González FG, Slafer GA, Miralles DJ (2003) Grain and floret number in response to photoperiod during stem elongation in fully and slightly vernalized wheats. Field Crops Research 81, 17–27.
| Grain and floret number in response to photoperiod during stem elongation in fully and slightly vernalized wheats.Crossref | GoogleScholarGoogle Scholar |
González FG, Slafer GA, Miralles DJ (2005a) Photoperiod during stem elongation in wheat: is its impact on fertile floret and grain number determination similar to that of radiation? Functional Plant Biology 32, 181–188.
| Photoperiod during stem elongation in wheat: is its impact on fertile floret and grain number determination similar to that of radiation?Crossref | GoogleScholarGoogle Scholar |
González FG, Slafer GA, Miralles DJ (2005b) Pre-anthesis development and number of fertile florets in wheat as affected by photoperiod sensitivity genes Ppd-D1 and Ppd-B1. Euphytica 146, 253–269.
| Pre-anthesis development and number of fertile florets in wheat as affected by photoperiod sensitivity genes Ppd-D1 and Ppd-B1.Crossref | GoogleScholarGoogle Scholar |
González FG, Miralles DJ, Slafer GA (2011) Wheat floret survival as related to pre-anthesis spike growth. Journal of Experimental Botany 62, 4889–4901.
| Wheat floret survival as related to pre-anthesis spike growth.Crossref | GoogleScholarGoogle Scholar |
Halloran GH, Pennell AL (1982) Duration and rate of development phases in wheat in two environments. Annals of Botany 49, 115–121.
| Duration and rate of development phases in wheat in two environments.Crossref | GoogleScholarGoogle Scholar |
Halse NJ, Weir RN (1970) Effects of vernalization, photoperiod and temperature on phenological development and spikelet number of Australian wheat. Australian Journal of Agricultural Research 21, 383–393.
| Effects of vernalization, photoperiod and temperature on phenological development and spikelet number of Australian wheat.Crossref | GoogleScholarGoogle Scholar |
Haun JR (1973) Visual quantification of wheat development. Agronomy Journal 65, 116–119.
| Visual quantification of wheat development.Crossref | GoogleScholarGoogle Scholar |
IPCC (2014) Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the fifth assessment report of the Intergovernmental Panel on Climate Change. Eds RK Pachauri, LA Meyer. IPCC, Geneva, Switzerland.
Islam-Faridi NM, Worland AJ, Law CN (1996) Inhibition of ear-emergence time and sensitivity to day-length determined by the group 6 chromosomes of wheat. Heredity 77, 572–580.
| Inhibition of ear-emergence time and sensitivity to day-length determined by the group 6 chromosomes of wheat.Crossref | GoogleScholarGoogle Scholar |
Kamran A, Iqbal M, Spaner D (2014) Flowering time in wheat (Triticum aestivum L.): a key factor for global adaptability. Euphytica 197, 1–26.
| Flowering time in wheat (Triticum aestivum L.): a key factor for global adaptability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisVCqurc%3D&md5=489951d140bd8c93e3a996477993311aCAS |
Khlestkina EK, Giura A, Röder MS, Börner A (2009) A new gene controlling the flowering response to photoperiod in wheat. Euphytica 165, 579–585.
| A new gene controlling the flowering response to photoperiod in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFCmsLjP&md5=1e6727654721e6c1a8ea3f4eefba9fcfCAS |
Kirby EJM, Appleyard M (1981) ‘Cereal development guide.’ (1st edn) (Cereal Unit, National Agricultural Centre: Warwickshire, UK)
Kiss T, Balla K, Veisz O, Láng L, Bedö Z, Griffiths S, Isaac P, Karsai I (2014) Allele frequencies in the VRN-A1, VRN-B1 and VRN-D1 vernalization response and PPD-B1 and PPD-D1 photoperiod sensitivity genes, and their effects on heading in a diverse set of wheat cultivars (Triticum aestivum L.). Molecular Breeding 34, 297–310.
| Allele frequencies in the VRN-A1, VRN-B1 and VRN-D1 vernalization response and PPD-B1 and PPD-D1 photoperiod sensitivity genes, and their effects on heading in a diverse set of wheat cultivars (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFCqt7%2FJ&md5=2c607988e5f26e5519be9bafd6902572CAS |
Langer SM, Longin CFH, Würschum T (2014) Flowering time control in European winter wheat. Frontiers in Plant Science 5, 1–11.
| Flowering time control in European winter wheat.Crossref | GoogleScholarGoogle Scholar |
Law CN, Sutka J, Worland AJ (1978) A genetic study of day-length response in wheat. Heredity 41, 185–191.
| A genetic study of day-length response in wheat.Crossref | GoogleScholarGoogle Scholar |
Law CN, Suarez E, Miller TE, Worland AJ (1998) The influence of the group 1 chromosomes of wheat on ear-emergence times and their involvement with vernalization and day length. Heredity 80, 83–91.
| The influence of the group 1 chromosomes of wheat on ear-emergence times and their involvement with vernalization and day length.Crossref | GoogleScholarGoogle Scholar |
Matsuyama H, Fujita M, Seki M, Kojima H, Shimazaki Y, Matsunaka H, Chono M, Hatta K, Kubo K, Takayama T, Kiribuchi-Otobe C, Oda S, Watanabe Y, Kato K (2015) Growth and yield properties of near-isogenic wheat lines carrying different photoperiodic response genes. Plant Production Science 18, 57–68.
| Growth and yield properties of near-isogenic wheat lines carrying different photoperiodic response genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntVOnu7s%3D&md5=ccec7f9e16ffa0c98e6557f8d34f24c2CAS |
McIntosh RA, Yamazaki Y, Devos KM, Dubcovsky J, Rogers WJ, Appels R (2003) Catalogue of gene symbols for wheat. In: Tenth International Wheat Genetics Symposium, 1–47.
Miglietta F (1989) Effect of photoperiod and temperature on leaf initiation rates in wheat (Triticum spp.). Field Crops Research 21, 121–130.
| Effect of photoperiod and temperature on leaf initiation rates in wheat (Triticum spp.).Crossref | GoogleScholarGoogle Scholar |
Miralles DJ, Richards RA (2000) Responses of leaf and tiller emergence and primordium initiation in wheat and barley to interchanged photoperiod. Annals of Botany 85, 655–663.
| Responses of leaf and tiller emergence and primordium initiation in wheat and barley to interchanged photoperiod.Crossref | GoogleScholarGoogle Scholar |
Miralles DJ, Richards RA, Slafer GA (2000) Duration of the stem elongation period influences the number of fertile florets in wheat and barley. Australian Journal of Plant Physiology 27, 931–940.
Miura H, Worland AJ (1994) Genetic control of vernalization, day-length response, and earliness per se by homoeologous group-3 chromosomes in wheat. Plant Breeding 113, 160–169.
| Genetic control of vernalization, day-length response, and earliness per se by homoeologous group-3 chromosomes in wheat.Crossref | GoogleScholarGoogle Scholar |
Muterko A, Kalendar R, Cockram J, Balashova I (2015) Discovery, evaluation and distribution of haplotypes and new alleles of the Photoperiod-A1 gene in wheat. Plant Molecular Biology 88, 149–164.
| Discovery, evaluation and distribution of haplotypes and new alleles of the Photoperiod-A1 gene in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmt1yqtb4%3D&md5=7e4b18d9ae12de87a895b2ee552488d3CAS |
Nishida H, Yoshida T, Kawakami K, Fujita M, Long B, Akashi Y, Laurie DA, Kato K (2013) Structural variation in the 5ʹ upstream region of photoperiod-insensitive alleles Ppd-A1a and Ppd-B1a identified in hexaploid wheat (Triticum aestivum L.), and their effect on heading time. Molecular Breeding 31, 27–37.
| Structural variation in the 5ʹ upstream region of photoperiod-insensitive alleles Ppd-A1a and Ppd-B1a identified in hexaploid wheat (Triticum aestivum L.), and their effect on heading time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvVWrtw%3D%3D&md5=36281be40654c2e64c9e92091af8ab60CAS |
Pugsley AT (1966) The photoperiodic sensitivity of some spring wheats with special reference to the variety thatcher. Australian Journal of Agricultural Research 17, 591–599.
| The photoperiodic sensitivity of some spring wheats with special reference to the variety thatcher.Crossref | GoogleScholarGoogle Scholar |
Rahman MS (1980) Effect of photoperiod and vernalization on the rate of development and spikelet number per ear in 30 varieties of wheat. Journal of the Australian Institute of Agricultural Science 46, 68–70.
Scarth R, Law CN (1983) The location of the photoperiod gene, Ppd2 and additional genetic factor for ear-emergence time on chromosome 2B of wheat. Heredity 51, 607–619.
| The location of the photoperiod gene, Ppd2 and additional genetic factor for ear-emergence time on chromosome 2B of wheat.Crossref | GoogleScholarGoogle Scholar |
Scarth R, Law CN (1984) The control of the day-length response in wheat by the group 2 chromosomes. Zeitschrift für Pflanzenzüchtung 92, 140–150.
Scarth R, Kirby EJM, Law CN (1985) Effects of the photoperiod genes Ppd1 and Ppd2 on growth and development of the shoot apex in wheat. Annals of Botany 55, 351–359.
| Effects of the photoperiod genes Ppd1 and Ppd2 on growth and development of the shoot apex in wheat.Crossref | GoogleScholarGoogle Scholar |
Shaw LM, Turner AS, Laurie DA (2012) The impact of photoperiod insensitive Ppd-1a mutations on the photoperiod pathway across the three genomes of hexaploid wheat (Triticum aestivum). The Plant Journal 71, 71–84.
| The impact of photoperiod insensitive Ppd-1a mutations on the photoperiod pathway across the three genomes of hexaploid wheat (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1GqurbK&md5=69f4dcb7624f5405dab35957603d433eCAS |
Slafer GA (2012) Wheat development: its role in phenotyping and improving crop adaptation. In ‘Physiological breeding I: interdisciplinary approaches to improve crop adaptation’. (Eds MP Reynolds, AJD Pask, DM Mullan) pp. 107–121. (CIMMYT: Mexico-Veracruz, Mexico)
Slafer GA, Rawson HM (1994a) Sensitivity of wheat phasic development to major environmental factors: A Re-examination of some assumptions made by physiologists and modellers. Australian Journal of Plant Physiology 21, 393–426.
| Sensitivity of wheat phasic development to major environmental factors: A Re-examination of some assumptions made by physiologists and modellers.Crossref | GoogleScholarGoogle Scholar |
Slafer GA, Rawson HM (1994b) Does temperature affect final numbers of primordia in wheat? Field Crops Research 39, 111–117.
| Does temperature affect final numbers of primordia in wheat?Crossref | GoogleScholarGoogle Scholar |
Slafer GA, Rawson HM (1995) Development in wheat as affected by timing and length of exposure to long photoperiod. Journal of Experimental Botany 46, 1877–1886.
| Development in wheat as affected by timing and length of exposure to long photoperiod.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlsFensQ%3D%3D&md5=df29fb7b54b9311286df9a2495431557CAS |
Slafer GA, Rawson HM (1996) Responses to photoperiod change with phenophase and temperature during wheat development. Field Crops Research 46, 1–13.
| Responses to photoperiod change with phenophase and temperature during wheat development.Crossref | GoogleScholarGoogle Scholar |
Slafer GA, Calderini DF, Miralles DJ (1996) Yield components and compensation in wheat: opportunities for further increasing yield potential. In ‘Increasing yield potential in wheat’. (Eds MP Reynolds, S Rajaram, A McNab) pp. 101–133. (CIMMYT: Mexico-Veracruz, Mexico)
Slafer GA, Abeledo LG, Miralles DJ, González FG, Whitechurch E (2001) Photoperiod sensitivity during stem elongation as an avenue to raise potential yield in wheat. Euphytica 119, 191–197.
| Photoperiod sensitivity during stem elongation as an avenue to raise potential yield in wheat.Crossref | GoogleScholarGoogle Scholar |
Snape JW, Butterworth K, Whitechurch E, Worland AJ (2001) Waiting for fine times: genetics of flowering time in wheat. Euphytica 119, 185–190.
| Waiting for fine times: genetics of flowering time in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvVemu7o%3D&md5=6dc9dd5bf76e6af3b81d10b128359ee2CAS |
Stelmakh AF (1997) Genetic systems regulating flowering response in wheat. In ‘Wheat: prospects for global improvement. Proceedings of the 5th international wheat conference, Turkey’. (Eds HJ Braun, F Altay, WE Kronstad) pp. 491–501. (Springer: Dordrecht, The Netherlands)
Tanio M, Kato K (2007) Development of near-isogenic lines for photoperiod-insensitive genes, Ppd-B1 and Ppd-D1, carried by the Japanese wheat cultivars and their effect on apical development. Breeding Science 57, 65–72.
| Development of near-isogenic lines for photoperiod-insensitive genes, Ppd-B1 and Ppd-D1, carried by the Japanese wheat cultivars and their effect on apical development.Crossref | GoogleScholarGoogle Scholar |
Turner AS, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310, 1031–1034.
| The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtF2is7nE&md5=687719cfb5e0dd902a9e8f98c6c55d83CAS |
Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnology Journal 8, 749–771.
| Plant responses to cold: transcriptome analysis of wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFKktrrJ&md5=21b4f619a74d7c66ee7dd757fb788dd1CAS |
Whitechurch EM, Slafer GA (2002) Contrasting Ppd alleles in wheat: effects on sensitivity to photoperiod in different phases. Field Crops Research 73, 95–105.
| Contrasting Ppd alleles in wheat: effects on sensitivity to photoperiod in different phases.Crossref | GoogleScholarGoogle Scholar |
Worland AJ (1996) The influence of flowering time genes on environmental adaptability in European wheats. Euphytica 89, 49–57.
| The influence of flowering time genes on environmental adaptability in European wheats.Crossref | GoogleScholarGoogle Scholar |
Zadoks JC, Chan TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Research 14, 415–421.
| A decimal code for the growth stages of cereals.Crossref | GoogleScholarGoogle Scholar |
