Achieving Phytonutrient Enhancement in a Potato by Breeding for

Chapter 8

Achieving Phytonutrient Enhancement in a Potato by Breeding for Increased Pigment 1

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Charles R. Brown , David Culley , Ronald E. Wrolstad , and Robert W. Durst

Downloaded by UNIV OF LIVERPOOL on May 14, 2018 | https://pubs.acs.org Publication Date: June 13, 2008 | doi: 10.1021/bk-2008-0983.ch008

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Agricultural Research Service, U.S. Department of Agriculture, Prosser, WA 99350 Batelle Pacific Northwest Laboratory, Richland, WA 99352 Department of Food Science and Technology, Oregon State University, Corvallis, OR 97331 2

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Potatoes have great genetic diversity in content and type of anthocyanins and carotenoids. Both pigment types are antioxidants. The carotenoids in potato are the same as those in the human retina and have been implicated as nutritional therapies for macular degeneration and cataracts. Anthocyanins, which belong to the very large group of phenolic compounds, may function as nutritional antagonists to processes leading to heart disease and certain cancers. The content of carotenoids and anthocyanins shows a wide range, a level of variation that augurs well for development of varieties where the salient feature will be nutraceutical in nature.

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© 2008 American Chemical Society

Culver and Wrolstad; Color Quality of Fresh and Processed Foods ACS Symposium Series; American Chemical Society: Washington, DC, 2008.


103 The potato is a modified underground stem that should be classified as a vegetable. The content of nutrients is as varied as in the case of other vegetables and it should be judged along side other vegetables. Having originated in South America, it was not known outside of this continent until European contact and colonization. Today there is still a large and highly genetically variable germplasm under cultivation in South America and residing in various collections around the world. One of the features of cultivars grown in the center of origin is the high frequency of pigmented skin and flesh compared to the modern varieties developed outside of the point of origin. It is not commonly known, for instance, that potatoes contain carotenoids, lutein and zeaxanthin, which are constituents of the human retina. Carotenoids have been found to stimulate processes involved in the immune system of animal models (/), and lutein has been found to inhibit breast cancer development in mice (2). Anthocyanins are present in the skin and flesh of potatoes and like other phenolic compounds the amount present in the diet is correlated with lower incidences of heart disease and cancer (3, 4). Both carotenoids and anthocyanins are antioxidants.

Genetics of Anthocyanins and Carotenoids in Potato The natural variation of cultivated potato germplasm includes types that are red and purple pigmented due to the presence of flavonoids in the skin and/or flesh. Anthocyanins are among the many flavonoids that may be found in potato tubers. A series of single genes control presence and absence of red and blue pigments. Different genetic systems controlling pigment expression have been identified for diploid cultivated versus tetraploid cultivated potatoes, (5, 6, 7). De Jong (8) and Van Eck and co-workers (9) have argued that the genes appear to be synthetic and should be regarded as belonging to one genome. The symbol D denotes a single gene controlling synthesis of red pigment, located on chromosome 2; the symbol P stands for a single gene on chromosome 11 controlling blue pigment synthesis, while I, of undetermined location, epistatically controls presence and absence of tuber skin and flesh pigmentation even when P and D are present. Gebhardt et al. (10) reported a locus controlling purple skin color, Psc, on chromosome 4. The single gene Pf, linked to I, determines whether pigment is present beyond the periderm in the interior tissues of the tuber (8, 9, 11). The pigments have been determined to be various types of acylated anthocyanidin glycosides (12, 13). The gene Ac is imputed to control acylation of anthocyanins. Diploid cultivated potatoes display both acylated and non-acylated forms while only acylated anthocyanins are present in the tetraploid cultivars (14). Potatoes have acylated glucosides of several aglycons: pelargonidin, petunidin, malvidin, and peonidin. Although genetic control of presence and absence of anthocyanins is monogenic, the completeness



104 of anthocyanin distribution in pigmented flesh may be under complex genetic control (8, 15). Outside of the center of origin of cultivated potato in the Andes of South America, it is rare to find varieties with anthocyanin pigments conferring red or purple flesh. However much of the world's production is occupied by yellow flesh potatoes which have higher total carotenoid than the white flesh varieties of North America and Great Britain. Potatoes synthesize and store in the tuber flesh xanthophyll type carotenoids, including predominantly lutein, violaxanthin and zeaxanthin (13, 15, 16, 17, 18, 19). White versus yellow flesh is thought to be under single gene control, while gene maps agree on the placement of this yellow flesh factor (Y/y) on homolog 3 (10, 20). White and yellow flesh potatoes have similar composition of carotenoids, however the yellow color of the latter group is due to higher concentrations of certain xanthophylls (21, 22). Evidence points to a gene encoding beta-carotene hydroxylase (BH) as the putative candidate for the Y/y gene. In Papa Amarilla germplasm, discussed later, an allele of BH shows significant regression with total carotenoid content with an R = 0.46 (23). 2

Carotenoid Content in Potato White and yellow flesh potato have xanthophyllous carotenoids. Yellow color intensity is a determinant of xanthophyll content up to a point. In Figure 1 we see the relationship of a Yellow Index (24) to the concentration of total carotenoids. Up to about 1000 ug per 100 g FW yellowness is correlated with content, but above these levels no further increase in yellowness is measured.

0

1000

2000

3000

Total Carotenoid (micrograms per 100 g FW)

Figure 1. Relationship of yellow index to total carotenoid content



105 The total carotenoid content of white cultivars and breeding lines ranges from 50 to 100 ug per 100 g FW. Yellow flesh cultivars may have contents ranging up to 270 ug, while more intensely yellow breeding clones are will range up to 800 (Table I). Although it is sometimes not directly observable, solidly red or purple flesh due to high anthocyanin concentration may be accompanied by higher total carotenoids as was noted in the red-yellow flesh clones in Table I. Levels of total carotenoid exceeding 2000 ug per 100 g FW have been reported in a number of studies (22, 23, 25). There is a class of potato cultivars in South America called Papa Amarilla (PA)(= yellow potato) which have exceedingly high carotenoid values. We have found that certain crosses made between PA parents produce progeny that exceed either of the parents by more than two population standard deviations (Figure 2). Three progeny exceeded 2, 400 ug per 100 g FW despite the fact that the mid parent value is 900 ug. This is an indication of transgressive segregation. It also indicates that it may be possible to breed intensely yellow cultivars with exceptionally high levels of total carotenoids.

Anthocyanin Content in Potato Anthocyanins are red to purple pigments ubiquitous in the plant kingdom. Anthocyanins are water soluble and are potent antioxidants. The general public

Figure 2. Distribution of total carotenoids contents in progeny of a cross between two Papa Amarilla types (91E22 and Yema de Huevo [= Egg Yolk]


106 Table I. Total carotenoid content in yellow and white flesh named varieties and experimental lines Cultivar or Breeding line Skin/Flesh Type


1

Light Yellow flesh cultivars and breeding lines Adora Divina Fabula Ilona Morning Gold Provento Satina Yukon Gold POR00PG4-2 Dark Yellow flesh breeding lines 91E22 PA99Pll-2 PA99P1-2 PA99P2-1 POR00PG4-1 Red and Yellow breeding lines POR00PG9-l POR00PG9-2 POR00PG9-3 POR00PG9-5 POR00PG9-6 White flesh cultivars and breeding lines Norkotah Ranger Burbank A8893-1 A9014-2 A90586-11 A9045-7 A90490-1 A91790-13 A92030-5 A93157-6LS Vw

W

W

Vw

w

Nw

w

w

Total Carotenoid jig/lOOgFW

Significance

W/Y W/Y W/Y W/Y W/Y W/Y W/Y W/Y W/Y

227 271 179 176 101 191 248 194 250

cdefg cdef cdefg cdefg defg cdefg cdefg cdefg cdefg

W/DY PR/DY PR/DY PR/DY W/DY

795 509 525 738 634

a b b a ab

PR/R&Y PR/R&Y PR/R&Y PR/R&Y PR/R&Y

299 307 109 273 327

cd cd defg cde c

RT/W RT/W RT/W RT/W RT/W RT/W RT/W RT/W RT/W RT/W RT/W

40 71 58 56 55 99 64 101 75 54 66

g efg fg g g defg efg defg efg g efg

NOTE: RT/W = russet skin/white flesh, W/Y = white skin/light yellow flesh, W/DY = white skin/dark yellow flesh, PR/R&Y = Partially red skin/red and yellow flesh, PR/DY = partially red skin/dark yellow flesh. Means not sharing the same letter are significantly different at the P < 0.05 level, using Duncan's Multiple Range Test.


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is familiar with red skin potatoes. The skin is red due to a high concentration of red anthocyanins in the epidermal layer. However, much higher levels of anthocyanins are present in the clones with pigmented flesh. The degree of pigmentation can vary from streaks or blotches of pigment generally associated with to solid dark degrees of pigment (Figure 3)

Figure 3. Different patterns and degrees of anthocyanin pigmentation in potato. The degree of pigmentation is under polygenic control, while presence and absence ofpigment in the flesh is under single gene control (See page 9 of color inserts.)

The concentration of anthocyanins can have a large range. The concentration of anthocyanin in skin tissue is quite high. However the skin is such a small volume of the whole tuber that generally a red skinned white fleshed potato has no more than 1.5 mg per 100 g FW when skin and flesh are extracted together. However, potatoes with anthocyanin in the flesh range from 15 to nearly 40 mg per lOOg FW (Table II). We have found that red flesh potatoes contain predominantly acylated glucosides of pelargonidin. Purple flesh potatoes have a more complex content of acylated glucosides of pelargonidin, petunidin, cyanidin, and malvidin (75). Red-skinned and purple-skinned potatoes are familiar in the marketplace. Pigmented flesh is new to people outside of the Andean countries of South America. The degree of pigmentation varies from flecks, lines and circles



Figure 4. HPLC separation of anthocyanin extracts from redflesh (A) and purple flesh potatoes (B). Peak 1 labeled in panel A, was identified by saponification, hydrolysis and HPLC analysis to be an acylated pelargonidin glucoside. Peaks 2 and 3 in panel B were identified by the same means as acylated glucosides of petunidin andpeonidin, respectively.


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associated with particular tuber tissues to solid pigmentation. The antioxidant potential of potatoes is correlated to the anthocyanin concentration. Other compounds are antioxidants and contribute to the total Oxygen Radical Absorbance Capacity (ORAC) (26) value. This is apparent in Figure 4 where the clones lacking any anthocyanin show a broad range of ORAC values.

S.9639x+ 115.01 0.7528

0.00

10.00

20.00

30.00

40.00

Anthocyanin content (mg/100 gfw)

Figure 5. Regression between anthocyanin content and antioxidant value (ORAC) is significant.

Breeding Objectives Development of new potato cultivars with specific non-traditional traits designed to appeal to a diet conscious populace is a relatively young endeavor. These potato have yet to find a steady market. However, the genetic diversity and nutritional bonuses embodied by the genetic diversity in pigment types and concentration have captured a faithful audience. Home gardeners, and small and large scale producers are watching this phenomenon. Ultimately the consumer will determine which direction the industry goes. However, selection programs are looking for attractive skin that retains a bright color even after extended storage. It appears that there is a market for below four ounce size tubers. At the same time, total yield is important, and it is likely that a high yield somewhat evenly divided between small and medium size tubers might be the most advantageous combination. It is likely that the crop destined for specialty markets will need to be closely managed for size. In this



Purple skin / Purple flesh PA97B29-2 P/P PA97B29-4 P/P PA97B29-6 P/P Red skin / red flesh NDOP5847-1 R/R PA97B35-1 R/R PA97B36-3 R/R PA97B37-7 R/R PA99P9-2 R/R

de cde de

a bede e abc abede

17.0 20.1 17.3 37.8 24.3 15.0 31.5 26.9

Nw

1420 1100 850 1410 1210

800 930 840

a abc be abc abc

c be be

Table II. Total anthocyanin and associated antioxidant levelhydrophilic Oxygen Radical Absorbance Capacity (ORAC) for purple flesh and red flesh breeding lines.



R/R R/R R/R R/R R/R R/R R/R R/R R/R R/R R/R

24.5 27.2 20.8 26.8 23.8 35.1 22.2 28.1 29.6 24.3 19.8

Means not sharing the same letter are significantly different using the Duncan's Multiple Range Test at P< 0.05

c abc abc be be be be abc abc abc be

Hydrophilic ORAC = trolox equivalents

790 1150 1040 980 850 1020 950 1160 1100 1160 1020

Vw

bcde abcde bcde abcde bcde ab bcde abcde abed bcde cde

Xy

^ Key to skin and tuber flesh types: R = red, P = purple.

PA99P9-4 PA99P10-2 PA99P20-1 PA99P20-2 PA99P32-5 POR00PG1-4 POR00PG2-1 POR00PG2-7 POR00PG2-11 POR00PG2-16 POR00PG3-1


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regard the overall yield is least likely to suffer if a heavy set of small tubers is the innate yield characteristic of the variety. Otherwise, the only way to limit size in more traditional plant types is to stop the growth by killing the foliage quite early in the growing season, reducing yield by a considerable amount. Consumers may prefer flesh pigmentation that maximizes nutritional benefits by having the highest possible concentration of anthocyanins or carotenoids. Alternatively, intriguing and attractive patterns of partial anthocyanin pigmentation may be highly appealing in fresh and processed products.

References 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19.

Lee, C.M.; Boileau, A. C.; Boileau, T. W. M.; Williams, A. W.; Swanson, K. S.; Heintz, K A.; Erdman, J. W. J. Nutr. 1999, 129, 2271-2277. Park, J. S.; Chew, B. P.; Wong, T. S. J. Nutr. 1998, 128, 1650-1656. Hertog, M. G. L.; Feskens, E.; Hollman, P.; Katan M.; Kromhout, D. Lancet 1993, 342, 1007-1011. Wang, H.; Nair, M. G.; Strasburg, G. M.; Chang, Y. C.; Booren, A. M.; Gray, J. I.; DeWitt, D. L. J. Nat. Prod. 1999, 62, 294-296. Dodds, K. S.; Long, D. H. J. Genetics 1955, 53, 136-149. Dodds, K. S.; Long, D. H. J. Genetics 1956, 54, 27-41. Lunden, A. P. Euphytica 1960, 9, 225-234. De Jong, H. Am. Potato J. 1991, 68, 585-593. Van Eck, H.J.; Jacobs, J. M. E.; Van den Berg, P. M. M. M.; Stiekema, M. J.; Jacobsen, E. Heredity 1994, 73, 410-421. Gebhardt, C.; Ritter, E.; Debener, T.; Schnachtschabel, U.; Walkemeier, B.; Uhrig, U.; Salamini, F. Theor. Appl. Genet. 1989, 78, 65-75. De Jong, H. Am. Potato J. 1987, 64, 337-343. Harbourne, J. B. Biochem. J. 1960, 74, 262-269. Rodriguez-Saona, L. E.; Giusti, M. M.; Wrolstad, R. E. J. Food Sci. 1998, 55,458-465. Swaminathan, M. S.; Howard, H. W. Bibliographia Genet. 1953, 16, 1. Brown, C. R.; Wrolstad, R.; Durst, R.; Yang, C.-P.; Clevidence, B. A. Am. J Potato Res. 2003, 80, 241-250. Fossen, T.; Andersen; Ø. M.. J. Hort. Sci. Biotechnol. 2000, 75, 360-363. Fossen, T; Øvstedal, D O.; Slimestad, R.; Andersen, Ø. M. Food Chem. 2003, 81, 433-437. Iwanzik W.; Tevini, M.;Stute, R.; Hilbert, R. Potato Res. 1983, 26, 149162. Mazza, G.; Miniati, E. Anthocyanins in Fruits, Vegetables and Grains. CRC Press: Boca Raton, FL, USA. 1993; pp 269-272.



113 20. Bonierbale, M. W.; Plaisted, R. L; Tanksley, S. D. Genetics 1988, 120, 1095-1103. 21. Gross, J. Pigments in Vegetables: Chlorophylls and Carotenoids. Van Nostrand Reinhold: New York, NY, USA. 1991; pp208-216. 22. Brown C. R.;Edwards, C. G.; Yang, C.-P.; Dean, B. B. J. Amer. Soc. Hort. Sci. 1993, 118, 145-150. 23. Brown, C. R; Kim, T.S.; Ganga, Z.; Haynes, K.; De Jong, D.; Jahn, M.; Paran, I.; De Jong, W. Am J. Potato Res. 2006, 83, 365-372. 24. Haynes, K. G.; Potts, W. E.; Chittams, J. L.; Fleck, D. L. J. Amer. Soc. Hort. Sci. 1994, 119, 1057-1059. 25. Lu, W.H.; Haynes, K.;Wiley, E.; Clevidence, B. J. Am. Soc. Hort. Sci. 2001, 126, 722-726. 26. Prior, R.L.; Cao,G. Free Radical Biol. and Med. 1999, 27, 1173-1181.


Achieving Phytonutrient Enhancement in a Potato by Breeding for

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