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Scientific Articles • Pesqui. Agropecu. Trop. 46 (4) • Oct-Dec 2016 • https://doi.org/10.1590/1983-40632016v4641811   copy

Inbreeding depression in crambe1

Depressão por endogamia em crambe

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Inbreeding depression in plants, caused by selfing or crossing among plants with a high degree of relatedness, is a genetic phenomenon that affects quantitative traits. This study aimed at verifying the occurrence of inbreeding depression in crambe progenies originated from selfing, in comparison with open pollination progenies. A randomized blocks design, with three replications, in a 32 x 2 factorial arrangement, with 32 crambe progenies and two reproduction systems (artificial selfing and open pollination), was used. Grain yield, 1,000-grain weight, plant height and final stand were evaluated. A significant interaction was observed between progenies and reproduction systems in all traits evaluated. A reduction in grain yield, 1,000-grain weight and plant height occurred in the majority of the selfing progenies, when compared to open pollination progenies. Inbreeding depression was observed in all traits, especially for grain yield. The heritability coefficients of selfed progenies were higher than the open pollinated ones, except for 1,000-grain weight.

KEYWORDS:
Crambe abyssinica Hochst; selfing; open pollination; heritability

RESUMO

A depressão por endogamia em plantas, causada por autofecundação ou cruzamento entre plantas com alto grau de parentesco, é um fenômeno genético que afeta os caracteres quantitativos. Objetivou-se verificar a ocorrência de depressão por endogamia em progênies de crambe originadas de autofecundação, em comparação com progênies de polinização livre. O delineamento experimental foi em blocos casualizados, com três repetições, em esquema fatorial 32 x 2, em que foram avaliadas 32 progênies de crambe sob dois sistemas de reprodução (autofecundação artificial e polinização livre). Foram avaliados a produtividade de grãos, massa de 1.000 grãos, altura de planta e estande final. Observou-se interação significativa entre progênies e sistemas de reprodução para todas as características avaliadas. Para a maioria das progênies, houve redução na produtividade de grãos, massa de 1.000 grãos e altura de plantas oriundas de autofecundação, em comparação com as progênies de polinização livre. Houve depressão por endogamia para todas as características avaliadas, especialmente para a produtividade de grãos. Os coeficientes de herdabilidade para as progênies oriundas de autofecundação foram maiores do que para as de polinização livre, exceto para massa de 1.000 grãos.

PALAVRAS-CHAVE:
Crambe abyssinica Hochst; autofecundação; polinização aberta; herdabilidade

INTRODUCTION

Crambe (Crambe abyssinica Hochst), a species of the Brassicaceae family (Desai et al. 1997DESAI, B. B. et al. Seeds handbook: biology, production, processing and storage. New York: Basel, 1997.), has attracted the interest of producers due to its short cycle and possibility of completely mechanized cultivation. This winter crop, a low-cost off-season alternative in Brazil, is planted after the soybean harvest (Pitol 2010PITOL, C.; BROCHI, D. L.; ROSCOE, R. Tecnologia e produção: crambe 2010. Maracajú: Fundação MS, 2010.). The seeds are its main raw material, containing approximately 37 % of oil (Glaser 1996GLASER, L. K. Crambe: an economic assessment of the feasibility of providing multiple-peril crop insurance. Washington, DC: Economic Research Service for the Risk Management Agency, 1996.) with 55-60 % of erucid acid (Lessman & Berry 1967LESSMAN, K. J.; BERRY, C. Crambe and vernonia research results at the forage farm in 1966. West Lafayette: Purdue University, 1967.), which may be used as an industrial lubricant, corrosion inhibitor or as an ingredient in synthetic rubber manufacturing. One of the products that may be obtained from the crambe oil is erucamide, an organic amide and erucic acid derivative that may be employed in cosmetics and other industrial uses (Falasca et al. 2010FALASCA, S. L. et al. Crambe abyssinica: an almost unknown crop with a promissory future to produce biodiesel in Argentina. International Journal of Hydrogen Energy, v. 35, n. 11, p. 5808-5812, 2010.).

The University of North Dakota (USA) has the most consistent crambe breeding program, where existing germplasm is evaluated and selection is made among and within populations developed through hybridization and subsequent selfing (Knights 2002KNIGHTS, S. Crambe: a North Dakota case study. Barton: Rural Industries Research and Development Corporation, 2002.). This breeding program makes assessments in all crop seasons by comparing newly selected lines with cultivars. In 2011, the North Dakota State University - Carrington Research Extension Center published the grain yield results (1,501.8-1,637.5 kg ha-1) for the BelAnn, Meyer and Westhope cultivars (NDSU 2011NORTH DAKOTA STATE UNIVERSITY (NDSU). Variety trial results 2011: Crambe. Available at: <https://www.ag.ndsu.edu/varietytrials/carrington-rec/2011-trial-results/2011crambe.pdf/view>. Acces on: 20 Dec. 2015.
https://www.ag.ndsu.edu/varietytrials/ca... ). In Brazil, the only existing crambe genotype is the FMS Brilhante cultivar, obtained by the Fundação MS, with grain yield of 1,400 kg ha-1 (Pitol 2010PITOL, C.; BROCHI, D. L.; ROSCOE, R. Tecnologia e produção: crambe 2010. Maracajú: Fundação MS, 2010.).

Lara-Fioreze et al. (2016)LARA-FIOREZE, A. C. C. et al. Genetic variation and gain in progenies of crambe. Crop Breeding and Applied Biotechnology, v. 16, n. 2, p. 132-140, 2016. carried out a selection process with the FMS Brilhante cultivar, obtaining a genetic gain of two-fold higher grain yields. It is, therefore, important that crambe breeding maintains the progress and development of new genetic materials. For that, knowledge on this crop, especially for traits related to the reproductive system, is crucial.

Although few studies have described crambe as a preferentially autogamous plant (Beck et al. 1975BECK, L. C. et al. Inheritance of pubescence and its use in outcrossing measurements between a Crambe hispanica type and C. abyssinica Hochst. Ex. R. E. Fries. Crop Science, v. 15, n. 2, p. 221-224, 1975.), intercrossing rates ranging 9-14 % have been previously reported (Vollmann & Ruckenbauer 1991VOLLMANN, J.; RUCKENBAUER, P. Estimation of outcrossing rates in crambe (Crambe abyssinica Hochst. Ex. R. E. Fries) using a dominant morphological marker gene. Die Bodenkultur, v. 42, n. 1, p. 361-366, 1991.).

The inbreeding phenomenon influences many quantitative traits and is related to increases in homozygosity at loci with some degree of dominance (Charlesworth & Charlesworth 1999CHARLESWORTH, B.; CHARLESWORTH, D. The genetic basis of inbreeding depression. Genetical Research, v. 74, n. 3, p. 329-340, 1999.). There are two genetically distinct ways in which increased homozygosity can lower fitness: increased homozygosity for partially recessive detrimental mutations and increased homozygosity for alleles at loci with heterozygote advantage ('overdominance'). Deleterious alleles will generally be present in populations at low frequencies (mutation-selection balance), whereas overdominant alleles at a locus are maintained at intermediate frequencies by balancing selection (Charlesworth & Willis 2009CHARLESWORTH, D.; WILLIS, J. The genetics of inbreeding depression. Nature Reviews Genetics, v. 10, n. 1, p. 783-796, 2009.). Darwin (1876DARWIN, C. R. The effects of cross and self-fertilization in the vegetable kingdom. London: John Murray, 1876. and 1877)DARWIN, C. R. The different forms of flowers on plants of the same species. London: John Murray, 1877. was the first to point out that the evident adaptations of many plants to ensure outcrossing could be understood in terms of the selective advantage of avoiding inbreeding depression.

In autogamous plants, inbreeding only results in loss of vigor in early generations (Allard 1999ALLARD, R. W. Principles of plant breeding. 2. ed. New York: Wiley, 1999.). This is not a disadvantage, since it causes the formation of different genotypic classes (dominant and recessive), increasing the possibility of selecting against recessive detrimental alleles.

Knowledge on inbreeding depression in crambe is important, since breeding occurs through selection among and within populations previously improved via hybridization and subsequent selfing. The method used to obtain pure lines in crambe is a combination of the "bulk" or population method and the "genealogic" or "pedigree" method (Knights 2002KNIGHTS, S. Crambe: a North Dakota case study. Barton: Rural Industries Research and Development Corporation, 2002.). These methods were implemented for autogamous plants, with outcrossing rates of less than 5 %. Moreover, studying the effects of inbreeding in crambe is important for the exploitation of heterosis and its possible use by the production of crambe hybrids.

Accordingly, this study aimed at verifying the occurrence of inbreeding depression in selfed crambe progenies, when compared to the respective open pollinated progenies.

MATERIAL AND METHODS

The experiment was performed with selected genotypes from the FMS Brilhante cultivar, which has shown to be a genetically heterogeneous cultivar (Lara-Fioreze et al. 2016LARA-FIOREZE, A. C. C. et al. Genetic variation and gain in progenies of crambe. Crop Breeding and Applied Biotechnology, v. 16, n. 2, p. 132-140, 2016.). In 2010, progenies of 32 superior genotypes of the FMS Brilhante were cultivated in 15-L pots filled with fertilized soil, under greenhouse conditions, in Botucatu, São Paulo State, Brazil. Each progeny was cultivated in five pots, with two plants per pot. At flowering, the inflorescences of five plants from each progeny were protected with a waterproof paper bag and the other five plants were open pollinated. The bags were maintained on the inflorescences until the fruit formation. At harvest, seeds from selfed and open pollinated progenies were collected separately.

In March 2011 (off-season), an experiment was conducted under field conditions, in Botucatu, in which a randomized blocks design, in a 32 x 2 factorial scheme, with three replications, was used. The factors consisted of 32 progenies and two means of reproduction (selfing and open pollination), obtained in the previous step. Sowing was carried out manually, and the experimental plot consisted of three 1-m rows with ten plants per row and spacing of 0.25 m between rows. The center row was the only one harvested. Planting and management, such as thinning, weed removal and harvest, were performed manually.

During the crop cycle, the following traits were evaluated in the crambe progenies: a) plant height: the height of ten plants in the center row, from the soil to the apical inflorescence, was measured using a ruler; b) final stand: the number of plants in the harvest row was counted before harvest; c) grain yield (kg ha-1): estimated as a function of the grain yield of each experimental plot (harvest row), corrected for a moisture content of 13 %; d) 1,000-grain weight: weight of eight replications of 100 seeds from each plot, taking the average of one hundred measurements, and converting the values to one thousand, using an analytical scale with accuracy of 0.001 g.

Because of the variability in the plant stand of the plots, grain yield data were corrected by covariance for the ideal stand (Cruz 1971CRUZ, V. F. Estudos sobre a correção de produção de parcelas em ensaios com milho. 1971. 143 f. Tese (Doutorado em Genética e Melhoramento) - Escola Superior de Agricultura Luiz de Queiroz, Piracicaba, 1971.). Based on the data obtained, variance analysis was performed using the F-test (p < 0.05), and the means were compared by the Scott-Knott test (p < 0.05) for all traits evaluated.

The inbreeding depression (ID) rates were obtained by comparing the average values of the open pollination and selfing progenies for the 32 genotypes, for all traits evaluated, according to the formula ID (%) = 100 - ((selfed * 100)/open pollination).

The genetic (σg2) and environmental (σe2) variances were estimated based on the mathematical expectations of the mean squares. The heritability coefficient was obtained according to the formula h2 = σg2/(σg2 + σe2).

All data were analyzed using the Genes software (Cruz 2001CRUZ, C. D. Genes software (version for windows): application in computational and statistical genetics.Viçosa: UFV, 2001.).

RESULTS AND DISCUSSION

Significant differences were observed for the sources of variation in all traits evaluated (Table 1). The mean square significance for means of reproduction shows differences between selfed and open pollinated progenies for all traits. The significant interaction between progenies and means of reproduction indicates that the crambe progenies did not respond similarly with respect to means of reproduction. This is interesting, because the progenies were all selected from the same heterogeneous cultivar (Lara-Fioreze et al. 2016LARA-FIOREZE, A. C. C. et al. Genetic variation and gain in progenies of crambe. Crop Breeding and Applied Biotechnology, v. 16, n. 2, p. 132-140, 2016.). In autogamous species, a homogeneous phenotype between progenies is expected as an effect of the homozygous loci. However, that was not observed in this study.

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Table 1
Mean squares for plant height, final stand, grain yield and 1,000-grain weight, in crambe progenies obtained using two means of reproduction (selfing and open pollination).

For plant height, the progenies 10, 11, 13, 18, 23, 24, 26, 28, 29, 30, 31 and 32 obtained the highest values in open pollination (Table 2). The decrease in plant height in selfed plants was first described by East & Hayes (1912)EAST, E. M.; HAYES, H. K. Heterozygosis in evolution and in plant breeding. Washington, DC: USDA, 1912., when studying corn.

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Table 2
Average values for plant height, final stand, grain yield and 1,000-grain weight of crambe progenies from two means of reproduction (selfing and open pollination) and their respective inbreeding depressions (ID).

In crambe, as well as in other crops, plant height is a very important trait, particularly for mechanical harvesting. Moreover, for being an herbaceous plant, whose branches form near the base (Desai et al. 1997DESAI, B. B. et al. Seeds handbook: biology, production, processing and storage. New York: Basel, 1997.), plant height is positively correlated with grain yield (Cargnelutti Filho et al. 2010CARGNELUTTI FILHO, A. et al. Tamanho de amostra e relações lineares de caracteres morfológicos e produtivos de crambe. Ciência Rural, v. 40, n. 11, p. 2262-2267, 2010.).

The selfed progenies 1, 3, 7, 12, 16, 22, 24, 26, 27, 28 and 29 showed a significant reduction in the final stand, when compared with their open pollinated counterparts. However, the selfed progenies 6 and 30 exhibited an opposite response, showing a higher final stand (Table 2).

A higher final stand may be related to two causes: higher germination or higher plant survival. Nevertheless, according to Baskin & Baskin (2015)BASKIN, J. M.; BASKIN, C. C. Inbreeding depression and the cost of inbreeding on seed germination. Seed Science, v. 25, n. 4, p. 355-385, 2015., it did not seem to be a strong relationship between a decrease in germination and an increase in the coefficient of inbreeding (F), in 743 species studied.

For grain yield, only the progenies 2, 8, 14 and 17 showed no significant differences between selfed and open pollinated plants. The progenies 13, 16, 20 and 30 showed a statistically lower 1,000-grain weight in selfed progenies. Only the selfed progeny 4 exhibited a statistically higher 1,000-grain weight than that of the open pollinated progeny. In general, the average grain yield values were lower in selfed progenies (Table 2).

There are two hypothesis for inbreeding depression: first that favorable alleles tend to be dominant or partially dominant, and second that heterozygotes have a higher phenotypic value than homozygotes (Crow & Kimura 1970CROW, J. F.; KIMURA, M. An introduction to population genetics theory. New York: Harper & Row, 1970.). According to Allard (1960)ALLARD, R. W. Principles of plant breeding.New York: Wiley, 1960. and Falconer (1987)FALCONER, D. S. Introduction to quantitative genetic. Viçosa: UFV, 1987., the theory of partial dominance states that dominance in alleles causes a difference between the phenotypic values ​​of homozygotes and heterozygotes, emphasizing that the depression caused by inbreeding is proportional to the degree of dominance. Inbreeding depression is also higher for loci with uniform allele frequencies. Thus, since the quantitative traits are controlled by many loci, a decline in the phenotypic value of this characteristic will also depend on the average degree of dominance that controls it.

Falconer (1987)FALCONER, D. S. Introduction to quantitative genetic. Viçosa: UFV, 1987. reports that the highest levels of inbreeding depression are expected in populations with high heterozygous frequencies in loci with gene dominance, such as in hybrids, and in populations with high genetic load, such as those that have not been improved. Based on the results obtained, it is likely that the population from which the progenies originated is only slightly improved and may also contain high genetic load.

The effect of inbreeding depression in crambe progenies may be observed in Table 2. The mean values of inbreeding depression ranged from 2.5 % (1,000-grain weight) to 64.9 % (grain yield). Moreover, the range of variation in inbreeding depression (positive values) and the absence of inbreeding depression (negative values) demonstrate the genetic variability among the crambe progenies for the traits evaluated.

Although crambe is considered an autogamous plant, our results indicate that the allogamy rate of the population used in this study is greater than in other genotypes evaluated previously, showing a mixed reproductive system. In this regard, one hypothesis to explain the occurrence of mixed-mating populations, in which individuals produce both self and outcrossed progeny, is that they are in an evolutionary transition from outcrossing to selfing. If purging is fast, the evolutionary transition from outcrossing to selfing should occur quickly, and mixed mating populations should become rare. According to Goodwillie et al. (2005)GOODWILLIE, C. et al. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology, Evolution and Systematics, v. 36, n. 1, p. 47-79, 2005., a recent tally of mating-system estimates for 345 plant species revealed that 42 % exhibited mixed mating, defined as selfing rates between 20 % and 80 %.

It is important to underscore that the population from which the progenies were selected was not genetically improved. Our results suggest that both the large variation in inbreeding depression and high inbreeding depression values show that evolutionary processes may still be acting and that the inbreeding depression may decrease over time. Charlesworth & Charlesworth (1987)CHARLESWORTH, D.; CHARLESWORTH, B. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology System, v. 18, n. 1, p. 237-268, 1987. report that self-fertilization exposes these mutations to selection, thereby reducing the magnitude of inbreeding depression. Moreover, species with intermediate selfing rates maintain a substantial inbreeding depression, comparable to that of predominantly outcrossing species (Winn et al. 2011WINN, A. et al. Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution, v. 65, n. 12, p. 3339-3359, 2011.). Therefore, the population may exhibit mixed mating.

Inbreeding is not always disadvantageous, because it leads to greater genetic variance among progenies and may increase the expected genetic gain with selection (Paterniani & Miranda 1987PATERNIANI, E.; MIRANDA FILHO, J. B. Populations breeding. In: PATERNIANI, E.; VIEGAS, G. P. (Eds.). Breeding and population of corn. Campinas: Fundação Cargill, 1987. p. 217-264.). The genetic variance was higher in the selfed progenies, if compared with the open pollinated ones (Table 3). Consequently, the estimated heritability coefficients for plant height, final stand, grain yield and 1,000-grain weight showed differences between the selfed and open pollinated progenies. The heritability coefficients were generally higher in selfed progenies, except for 1,000-grain weight.

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Table 3
Estimates of genetic parameters in selfed and open pollinated progenies of crambe.

The heritability coefficient expresses how much of the observed phenotypic variance is due to genetics, rather than environmental. For 1,000-grain weight, although the genetic variance of the selfed progenies was higher than in open pollinated progenies, the environmental variance was higher in the later. This result indicates a greater influence of the environment on the traits of open pollinated progenies, resulting in significantly lower heritability.

Although selfing may cause a loss of initial vigor in some traits with a higher degree of dominance or in slightly improved populations with high genetic load, it is important for the genetic load to be dissipated. Therefore, inbreeding in plants may be beneficial in breeding programs. Moreover, speculation on the means of reproduction of crambe is extremely important, and since the inbreeding depression observed is related to high allogamy rates, the breeding methods used should be adapted, with effective control of cross-fertilization at certain stages of breeding. Thus, further studies should be conducted to determine the allogamy rate that occurs in crambe under different environmental conditions.

CONCLUSIONS

  1. Crambe has marked inbreeding depression, with a variable rate among the evaluated progenies;

  2. The superior phenotype of open pollinated progenies, when compared to the selfed ones, indicates that crambe is not a selfing species and, probably, has a mixed mating system;

  3. The highest inbreeding depression observed is for grain yield.

REFERENCES

  • ALLARD, R. W. Principles of plant breedingNew York: Wiley, 1960.
  • ALLARD, R. W. Principles of plant breeding 2. ed. New York: Wiley, 1999.
  • BASKIN, J. M.; BASKIN, C. C. Inbreeding depression and the cost of inbreeding on seed germination. Seed Science, v. 25, n. 4, p. 355-385, 2015.
  • BECK, L. C. et al. Inheritance of pubescence and its use in outcrossing measurements between a Crambe hispanica type and C. abyssinica Hochst. Ex. R. E. Fries. Crop Science, v. 15, n. 2, p. 221-224, 1975.
  • CARGNELUTTI FILHO, A. et al. Tamanho de amostra e relações lineares de caracteres morfológicos e produtivos de crambe. Ciência Rural, v. 40, n. 11, p. 2262-2267, 2010.
  • CHARLESWORTH, D.; CHARLESWORTH, B. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology System, v. 18, n. 1, p. 237-268, 1987.
  • CHARLESWORTH, B.; CHARLESWORTH, D. The genetic basis of inbreeding depression. Genetical Research, v. 74, n. 3, p. 329-340, 1999.
  • CHARLESWORTH, D.; WILLIS, J. The genetics of inbreeding depression. Nature Reviews Genetics, v. 10, n. 1, p. 783-796, 2009.
  • CROW, J. F.; KIMURA, M. An introduction to population genetics theory New York: Harper & Row, 1970.
  • CRUZ, C. D. Genes software (version for windows): application in computational and statistical genetics.Viçosa: UFV, 2001.
  • CRUZ, V. F. Estudos sobre a correção de produção de parcelas em ensaios com milho 1971. 143 f. Tese (Doutorado em Genética e Melhoramento) - Escola Superior de Agricultura Luiz de Queiroz, Piracicaba, 1971.
  • DARWIN, C. R. The effects of cross and self-fertilization in the vegetable kingdom London: John Murray, 1876.
  • DARWIN, C. R. The different forms of flowers on plants of the same species. London: John Murray, 1877.
  • DESAI, B. B. et al. Seeds handbook: biology, production, processing and storage. New York: Basel, 1997.
  • EAST, E. M.; HAYES, H. K. Heterozygosis in evolution and in plant breeding Washington, DC: USDA, 1912.
  • FALASCA, S. L. et al. Crambe abyssinica: an almost unknown crop with a promissory future to produce biodiesel in Argentina. International Journal of Hydrogen Energy, v. 35, n. 11, p. 5808-5812, 2010.
  • FALCONER, D. S. Introduction to quantitative genetic Viçosa: UFV, 1987.
  • GLASER, L. K. Crambe: an economic assessment of the feasibility of providing multiple-peril crop insurance. Washington, DC: Economic Research Service for the Risk Management Agency, 1996.
  • GOODWILLIE, C. et al. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology, Evolution and Systematics, v. 36, n. 1, p. 47-79, 2005.
  • KNIGHTS, S. Crambe: a North Dakota case study. Barton: Rural Industries Research and Development Corporation, 2002.
  • LARA-FIOREZE, A. C. C. et al. Genetic variation and gain in progenies of crambe. Crop Breeding and Applied Biotechnology, v. 16, n. 2, p. 132-140, 2016.
  • LESSMAN, K. J.; BERRY, C. Crambe and vernonia research results at the forage farm in 1966 West Lafayette: Purdue University, 1967.
  • NORTH DAKOTA STATE UNIVERSITY (NDSU). Variety trial results 2011: Crambe. Available at: <https://www.ag.ndsu.edu/varietytrials/carrington-rec/2011-trial-results/2011crambe.pdf/view>. Acces on: 20 Dec. 2015.
    » https://www.ag.ndsu.edu/varietytrials/carrington-rec/2011-trial-results/2011crambe.pdf/view
  • PATERNIANI, E.; MIRANDA FILHO, J. B. Populations breeding. In: PATERNIANI, E.; VIEGAS, G. P. (Eds.). Breeding and population of corn Campinas: Fundação Cargill, 1987. p. 217-264.
  • PITOL, C.; BROCHI, D. L.; ROSCOE, R. Tecnologia e produção: crambe 2010. Maracajú: Fundação MS, 2010.
  • VOLLMANN, J.; RUCKENBAUER, P. Estimation of outcrossing rates in crambe (Crambe abyssinica Hochst. Ex. R. E. Fries) using a dominant morphological marker gene. Die Bodenkultur, v. 42, n. 1, p. 361-366, 1991.
  • WINN, A. et al. Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution, v. 65, n. 12, p. 3339-3359, 2011.

Publication Dates

  • Publication in this collection
    Oct-Dec 2016

History

  • Received
    June 2016
  • Accepted
    Nov 2016
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