Delayed greening in phosphorus-efficient Hakea prostrata (Proteaceae) is a photoprotective and nutrient-saving strategy
Thirumurugen Kuppusamy
A C , Dorothee Hahne B , Kosala Ranathunge A , Hans Lambers A and Patrick M. Finnegan A
+ Author Affiliations
- Author Affiliations
A School of Biological Sciences, The University of Western Australia, 35 Stirling Highway, Perth, WA 6009, Australia.
B Metabolomics Australia, Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, 35 Stirling Highway, Perth, WA 6009, Australia.
C Corresponding author. Email: skthikuppusamy@gmail.com
Functional Plant Biology 48(2) 218-230 https://doi.org/10.1071/FP19285
Submitted: 5 October 2019 Accepted: 18 September 2020 Published: 26 October 2020
Abstract
Hakea prostrata R.Br. (Proteaceae) shows a ‘delayed greening’ strategy of leaf development characterised by reddish young leaves that become green as they mature. This trait may contribute to efficient use of phosphorus (P) during leaf development by first investing P in the development of leaf structure followed by maturation of the photosynthetic machinery. In this study, we investigated the properties of delayed greening in a highly P-efficient species to enhance our understanding of the ecological significance of this trait as a nutrient-saving and photoprotective strategy. In glasshouse-grown plants, we assessed foliar pigments, fatty acids and nutrient composition across five leaf developmental stages. Young leaves had higher concentrations of anthocyanin, P, nitrogen (N), copper (Cu), xanthophyll-cycle pigments and saturated fatty acids than mature leaves. As leaves developed, the concentration of anthocyanins decreased, whereas that of chlorophyll and the double bond index of fatty acids increased. In mature leaves, ~60% of the fatty acids was α-linolenic acid (C18:3 n-3). Mature leaves also had higher concentrations of aluminium (Al), calcium (Ca) and manganese (Mn) than young leaves. We conclude that delayed greening in H. prostrata is a strategy that saves P as well as N and Cu through sequential allocation of these resources, first to cell production and structural development, and then to supplement chloroplast development. This strategy also protects young leaves against photodamage and oxidative stress during leaf expansion under high-light conditions.
Keywords: anthocyanin, chlorophyll, delayed greening, fatty acids, Hakea prostrata, nitrogen, phosphorus, photodamage, violaxanthin cycle pigments.
References
Abrahão A, Ryan M, Laliberté E, Oliveira R, Lambers H (2018) Phosphorus- and nitrogen-acquisition strategies in two Bossiaea species (Fabaceae) along retrogressive soil chronosequences in south-western Australia. Physiologia Plantarum 163, 323–343.| Phosphorus- and nitrogen-acquisition strategies in two Bossiaea species (Fabaceae) along retrogressive soil chronosequences in south-western Australia.Crossref | GoogleScholarGoogle Scholar |
Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods in Enzymology 8, 115–118.
| Assay of inorganic phosphate, total phosphate and phosphatases.Crossref | GoogleScholarGoogle Scholar |
Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Frontiers in Plant Science 4, 273
| Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops.Crossref | GoogleScholarGoogle Scholar | 23914193PubMed |
Bromke MA, Hochmuth A, Tohge T, Fernie AR, Giavalisco P, Burgos A, Willmitzer L, Brotman Y (2015) Liquid chromatography high-resolution mass spectrometry for fatty acid profiling. The Plant Journal 81, 529–536.
| Liquid chromatography high-resolution mass spectrometry for fatty acid profiling.Crossref | GoogleScholarGoogle Scholar | 25440443PubMed |
Bungard RA, McNeil D, Morton JD (1997) Effects of nitrogen on the photosynthetic apparatus of Clematis vitalba grown at several irradiances. Australian Journal of Plant Physiology 24, 205–214.
| Effects of nitrogen on the photosynthetic apparatus of Clematis vitalba grown at several irradiances.Crossref | GoogleScholarGoogle Scholar |
Burger J, Edwards GE (1996) Photosynthetic efficiency, and photodamage by UV and visible radiation, in red versus green leaf Coleus varieties. Plant & Cell Physiology 37, 395–399.
| Photosynthetic efficiency, and photodamage by UV and visible radiation, in red versus green leaf Coleus varieties.Crossref | GoogleScholarGoogle Scholar |
Cai ZQ, Slot M, Fan ZX (2005) Leaf development and photosynthetic properties of three tropical tree species with delayed greening. Photosynthetica 43, 91–98.
| Leaf development and photosynthetic properties of three tropical tree species with delayed greening.Crossref | GoogleScholarGoogle Scholar |
Cazzaniga S, Bressan M, Carbonera D, Agostini A, Dall’Osto L (2016) Differential roles of carotenes and xanthophylls in photosystem I photoprotection. Biochemistry 55, 3636–3649.
| Differential roles of carotenes and xanthophylls in photosystem I photoprotection.Crossref | GoogleScholarGoogle Scholar | 27290879PubMed |
Cazzonelli CI (2011) Carotenoids in nature: insights from plants and beyond. Functional Plant Biology 38, 833–847.
| Carotenoids in nature: insights from plants and beyond.Crossref | GoogleScholarGoogle Scholar | 32480941PubMed |
Close DC, Beadle CL (2003) The ecophysiology of foliar anthocyanin. Botanical Review 69, 149–161.
| The ecophysiology of foliar anthocyanin.Crossref | GoogleScholarGoogle Scholar |
Coley PD, Aide TM (1989) Red coloration of tropical young leaves: a possible antifungal defence? Journal of Tropical Ecology 5, 293–300.
| Red coloration of tropical young leaves: a possible antifungal defence?Crossref | GoogleScholarGoogle Scholar |
Croce R, Weiss S, Bassi R (1999) Carotenoid-binding sites of the major light-harvesting complex II of higher plants. The Journal of Biological Chemistry 274, 29613–29623.
| Carotenoid-binding sites of the major light-harvesting complex II of higher plants.Crossref | GoogleScholarGoogle Scholar | 10514429PubMed |
Crombie WM (1958) Fatty acids in chloroplasts and leaves. Journal of Experimental Botany 9, 254–261.
| Fatty acids in chloroplasts and leaves.Crossref | GoogleScholarGoogle Scholar |
Czech AS, Strzałka K, Schurr U, Matsubara S (2009) Developmental stages of delayed-greening leaves inferred from measurements of chlorophyll content and leaf growth. Functional Plant Biology 36, 654–664.
| Developmental stages of delayed-greening leaves inferred from measurements of chlorophyll content and leaf growth.Crossref | GoogleScholarGoogle Scholar | 32688678PubMed |
de Araújo RP, de Almeida A-AF, Barroso JP, de Oliveira RA, Gomes FP, Ahnert D, Baligar V (2017) Molecular and morphophysiological responses cocoa leaves with different concentrations of anthocyanin to variations in light levels. Scientia Horticulturae 224, 188–197.
| Molecular and morphophysiological responses cocoa leaves with different concentrations of anthocyanin to variations in light levels.Crossref | GoogleScholarGoogle Scholar |
Esteban R, Becerril JM, García-Plazaola JI (2009a) Lutein epoxide cycle, more than just a forest tale. Plant Signaling & Behavior 4, 342–344.
| Lutein epoxide cycle, more than just a forest tale.Crossref | GoogleScholarGoogle Scholar |
Esteban R, Olano JM, Castresana J, Fernández-Marín B, Hernández A, Becerril JM, García-Plazaola JI (2009b) Distribution and evolutionary trends of photoprotective isoprenoids (xanthophylls and tocopherols) within the plant kingdom. Physiologia Plantarum 135, 379–389.
| Distribution and evolutionary trends of photoprotective isoprenoids (xanthophylls and tocopherols) within the plant kingdom.Crossref | GoogleScholarGoogle Scholar | 19210752PubMed |
Falcone Ferreyra ML, Rius S, Casati P (2012) Flavonoids: biosynthesis, biological functions, and biotechnological applications. Frontiers in Plant Science 3, 222
| Flavonoids: biosynthesis, biological functions, and biotechnological applications.Crossref | GoogleScholarGoogle Scholar | 23060891PubMed |
Färber A, Young A, Ruban A, Horton P, Jahns P (1997) Dynamics of xanthophyll-cycle activity in different antenna subcomplexes in the photosynthetic membranes of higher plants (The relationship between zeaxanthin conversion and nonphotochemical fluorescence quenching). Plant Physiology 115, 1609–1618.
| Dynamics of xanthophyll-cycle activity in different antenna subcomplexes in the photosynthetic membranes of higher plants (The relationship between zeaxanthin conversion and nonphotochemical fluorescence quenching).Crossref | GoogleScholarGoogle Scholar | 12223884PubMed |
Freeman Allen C, Good P, Davis HF, Fowler SD (1964) Plant and chloroplast lipids I. Separation and composition of major spinach lipids. Biochemical and Biophysical Research Communications 15, 424–430.
| Plant and chloroplast lipids I. Separation and composition of major spinach lipids.Crossref | GoogleScholarGoogle Scholar |
Gilmore AM, Björkman O (1994) Adenine nucleotides and the xanthophyll cycle in leaves. Planta 192, 537–544.
| Adenine nucleotides and the xanthophyll cycle in leaves.Crossref | GoogleScholarGoogle Scholar |
Gould KS (2004) Nature’s Swiss army knife: the diverse protective roles of anthocyanins in leaves. Journal of Biomedicine & Biotechnology 2004, 314–320.
| Nature’s Swiss army knife: the diverse protective roles of anthocyanins in leaves.Crossref | GoogleScholarGoogle Scholar |
Gould KS, Markham KR, Smith RH, Goris JJ (2000) Functional role of anthocyanins in the leaves of Quintinia serrata A. Cunn. Journal of Experimental Botany 51, 1107–1115.
| Functional role of anthocyanins in the leaves of Quintinia serrata A. Cunn.Crossref | GoogleScholarGoogle Scholar | 10948238PubMed |
Gould KS, Vogelmann TC, Han T, Clearwater MJ (2002) Profiles of photosynthesis within red and green leaves of Quintinia serrata. Physiologia Plantarum 116, 127–133.
| Profiles of photosynthesis within red and green leaves of Quintinia serrata.Crossref | GoogleScholarGoogle Scholar | 12207671PubMed |
Hayes PE, Clode PL, Oliveira RS, Lambers H (2018) Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells: an adaptation improving phosphorus-use efficiency. Plant, Cell & Environment 41, 605–619.
| Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells: an adaptation improving phosphorus-use efficiency.Crossref | GoogleScholarGoogle Scholar |
Hopper SD, Gioia P (2004) The Southwest Australian Floristic Region: evolution and conservation of a global hot spot of biodiversity. Annual Review of Ecology, Evolution, and Systematics 35, 623–650.
| The Southwest Australian Floristic Region: evolution and conservation of a global hot spot of biodiversity.Crossref | GoogleScholarGoogle Scholar |
Hu L, Bi A, Hu Z, Amombo E, Li H, Fu J (2018) Antioxidant metabolism, photosystem II, and fatty acid composition of two tall fescue genotypes with different heat tolerance under high temperature Stress. Frontiers in Plant Science 9, 1242
| Antioxidant metabolism, photosystem II, and fatty acid composition of two tall fescue genotypes with different heat tolerance under high temperature Stress.Crossref | GoogleScholarGoogle Scholar | 30186304PubMed |
Hughes NM, Carpenter KL, Keidel TS, Miller CN, Waters MN, Smith WK (2014) Photosynthetic costs and benefits of abaxial versus adaxial anthocyanins in Colocasia esculenta ‘Mojito’. Planta 240, 971–981.
| Photosynthetic costs and benefits of abaxial versus adaxial anthocyanins in Colocasia esculenta ‘Mojito’.Crossref | GoogleScholarGoogle Scholar | 24903360PubMed |
Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta 1817, 182–193.
| The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II.Crossref | GoogleScholarGoogle Scholar | 21565154PubMed |
Jahns P, Wehner A, Paulsen H, Hobe S (2001) De-epoxidation of violaxanthin after reconstitution into different carotenoid binding sites of light-harvesting complex II. Journal of Biological Chemistry 276, 22154–22159.
| De-epoxidation of violaxanthin after reconstitution into different carotenoid binding sites of light-harvesting complex II.Crossref | GoogleScholarGoogle Scholar | 11301335PubMed |
Jahns P, Latowski D, Strzalka K (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochimica et Biophysica Acta 1787, 3–14.
| Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids.Crossref | GoogleScholarGoogle Scholar | 18976630PubMed |
Jeong ML, Jiang H, Chen HS, Tsai CJ, Harding SA (2004) Metabolic profiling of the sink-to-source transition in developing leaves of quaking aspen. Plant Physiology 136, 3364–3375.
| Metabolic profiling of the sink-to-source transition in developing leaves of quaking aspen.Crossref | GoogleScholarGoogle Scholar | 15448196PubMed |
Kalve S, De Vos D, Beemster GTS (2014) Leaf development: a cellular perspective. Frontiers in Plant Science 5, 362
| Leaf development: a cellular perspective.Crossref | GoogleScholarGoogle Scholar | 25132838PubMed |
Karageorgou P, Manetas Y (2006) The importance of being red when young: anthocyanins and the protection of young leaves of Quercus coccifera from insect herbivory and excess light. Tree Physiology 26, 613–621.
| The importance of being red when young: anthocyanins and the protection of young leaves of Quercus coccifera from insect herbivory and excess light.Crossref | GoogleScholarGoogle Scholar | 16452075PubMed |
Kunst L, Browse J, Somerville C (1989) Enhanced thermal tolerance in a mutant of Arabidopsis deficient in palmitic acid unsaturation. Plant Physiology 91, 401
| Enhanced thermal tolerance in a mutant of Arabidopsis deficient in palmitic acid unsaturation.Crossref | GoogleScholarGoogle Scholar | 16667033PubMed |
Kuppusamy T, Giavalisco P, Arvidsson S, Sulpice R, Stitt M, Finnegan PM, Scheible WR, Lambers H, Jost R (2014) Lipid biosynthesis and protein concentration respond uniquely to phosphate supply during leaf development in highly phosphorus-efficient Hakea prostrata. Plant Physiology 166, 1891–1911.
| Lipid biosynthesis and protein concentration respond uniquely to phosphate supply during leaf development in highly phosphorus-efficient Hakea prostrata.Crossref | GoogleScholarGoogle Scholar | 25315604PubMed |
Kursar TA, Coley PD (1991) Nitrogen content and expansion rate of young leaves of rain forest species: implications for herbivory. Biotropica 23, 141–150.
| Nitrogen content and expansion rate of young leaves of rain forest species: implications for herbivory.Crossref | GoogleScholarGoogle Scholar |
Kursar TA, Coley PD (1992a) The consequences of delayed greening during leaf development for light absorption and light use efficiency. Plant, Cell & Environment 15, 901–909.
| The consequences of delayed greening during leaf development for light absorption and light use efficiency.Crossref | GoogleScholarGoogle Scholar |
Kursar TA, Coley PD (1992b) Delayed greening in tropical leaves: an antiherbivore defense? Biotropica 24, 256–262.
| Delayed greening in tropical leaves: an antiherbivore defense?Crossref | GoogleScholarGoogle Scholar |
Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant and Soil 334, 11–31.
| Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies.Crossref | GoogleScholarGoogle Scholar |
Lambers H, Finnegan PM, Laliberte E, Pearse SJ, Ryan MH, Shane MW, Veneklaas EJ (2011) Update on phosphorus nutrition in Proteaceae. Phosphorus nutrition of proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiology 156, 1058–1066.
| Update on phosphorus nutrition in Proteaceae. Phosphorus nutrition of proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops?Crossref | GoogleScholarGoogle Scholar | 21498583PubMed |
Lambers H, Cawthray GR, Giavalisco P, Kuo J, Laliberté E, Pearse SJ, Scheible WR, Stitt M, Teste F, Turner BL (2012) Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. New Phytologist 196, 1098–1108.
| Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency.Crossref | GoogleScholarGoogle Scholar | 22937909PubMed |
Lambers H, Finnegan PM, Jost R, Plaxton WC, Shane MW, Stitt M (2015) Phosphorus nutrition in Proteaceae and beyond. Nature Plants 1, 15109
| Phosphorus nutrition in Proteaceae and beyond.Crossref | GoogleScholarGoogle Scholar | 27250542PubMed |
Lim DKY, Garg S, Timmins M, Zhang ESB, Thomas-Hall SR, Schuhmann H, Li Y, Schenk PM (2012) Isolation and evaluation of oil-producing microalgae from subtropical coastal and brackish waters. PLoS One 7, e40751
| Isolation and evaluation of oil-producing microalgae from subtropical coastal and brackish waters.Crossref | GoogleScholarGoogle Scholar |
Liu X, Huang B (2004) Changes in fatty acid composition and saturation in leaves and roots of creeping bentgrass exposed to high soil temperature. Journal of the American Society for Horticultural Science 129, 795–801.
| Changes in fatty acid composition and saturation in leaves and roots of creeping bentgrass exposed to high soil temperature.Crossref | GoogleScholarGoogle Scholar |
Liu T, Ren T, White PJ, Cong R, Lu J (2018) Storage nitrogen co-ordinates leaf expansion and photosynthetic capacity in winter oilseed rape. Journal of Experimental Botany 69, 2995–3007.
| Storage nitrogen co-ordinates leaf expansion and photosynthetic capacity in winter oilseed rape.Crossref | GoogleScholarGoogle Scholar | 29669007PubMed |
Miyazawa SI, Makino A, Terashima I (2003) Changes in mesophyll anatomy and sink–source relationships during leaf development in Quercus glauca, an evergreen tree showing delayed leaf greening. Plant, Cell & Environment 26, 745–755.
| Changes in mesophyll anatomy and sink–source relationships during leaf development in Quercus glauca, an evergreen tree showing delayed leaf greening.Crossref | GoogleScholarGoogle Scholar |
Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Critical Reviews in Plant Sciences 21, 31–57.
| The function of tocopherols and tocotrienols in plants.Crossref | GoogleScholarGoogle Scholar |
Murakami Y, Tsuyama M, Kobayashi Y, Kodama H, Iba K (2000) Trienoic fatty acids and plant tolerance of high temperature. Science 287, 476
| Trienoic fatty acids and plant tolerance of high temperature.Crossref | GoogleScholarGoogle Scholar | 10642547PubMed |
Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Molecular Plant 8, 68–82.
| Carotenoid metabolism in plants.Crossref | GoogleScholarGoogle Scholar | 25578273PubMed |
Niyogi KK (2000) Safety valves for photosynthesis. Current Opinion in Plant Biology 3, 455–460.
| Safety valves for photosynthesis.Crossref | GoogleScholarGoogle Scholar | 11074375PubMed |
Niyogi KK, Bjorkman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proceedings of the National Academy of Sciences of the United States of America 94, 14162–14167.
| The roles of specific xanthophylls in photoprotection.Crossref | GoogleScholarGoogle Scholar | 9391170PubMed |
Prodhan MA, Jost R, Watanabe M, Hoefgen R, Lambers H, Finnegan PM (2016) Tight control of nitrate acquisition in a plant species that evolved in an extremely phosphorus‐impoverished environment. Plant, Cell & Environment 39, 2754–2761.
| Tight control of nitrate acquisition in a plant species that evolved in an extremely phosphorus‐impoverished environment.Crossref | GoogleScholarGoogle Scholar |
Prodhan MA, Finnegan PM, Lambers H (2019) How does evolution in phosphorus-impoverished landscapes impact plant nitrogen and sulfur assimilation? Trends in Plant Science 24, 69–82.
| How does evolution in phosphorus-impoverished landscapes impact plant nitrogen and sulfur assimilation?Crossref | GoogleScholarGoogle Scholar | 30522809PubMed |
Queenborough SA, Metz MR, Valencia R, Wright SJ (2013) Demographic consequences of chromatic leaf defence in tropical tree communities: do red young leaves increase growth and survival? Annals of Botany 112, 677–684.
| Demographic consequences of chromatic leaf defence in tropical tree communities: do red young leaves increase growth and survival?Crossref | GoogleScholarGoogle Scholar | 23881717PubMed |
Raven JA (2013) RNA function and phosphorus use by photosynthetic organisms. Frontiers in Plant Science 4, 536
| RNA function and phosphorus use by photosynthetic organisms.Crossref | GoogleScholarGoogle Scholar | 24421782PubMed |
Schmitt M, Watanabe T, Jansen S (2016) The effects of aluminium on plant growth in a temperate and deciduous aluminium accumulating species. AoB Plants 8, plw065
| The effects of aluminium on plant growth in a temperate and deciduous aluminium accumulating species.Crossref | GoogleScholarGoogle Scholar | 27613876PubMed |
Shane MW, Cramer MD, Funayama-Noguchi S, Cawthray GR, Millar AH, Day DA, Lambers H (2004) Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiology 135, 549–560.
| Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase.Crossref | GoogleScholarGoogle Scholar | 15122030PubMed |
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Le Journal de Botanique 2012, 217037
| Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions.Crossref | GoogleScholarGoogle Scholar |
Sulpice R, Ishihara H, Schlereth A, Cawthray GR, Encke B, Giavalisco P, Ivakov A, Arrivault S, Jost R, Krohn N, Kuo J, Laliberté E, Pearse SJ, Raven JA, Scheible W-R, Teste F, Veneklaas EJ, Stitt M, Lambers H (2014) Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. Plant, Cell & Environment 37, 1276–1298.
| Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species.Crossref | GoogleScholarGoogle Scholar |
Takaichi S, Mirauro M (1998) Distribution and geometric isomerism of neoxanthin in oxygenic phototrophs: 9′-cis, a sole molecular form. Plant & Cell Physiology 39, 968–977.
| Distribution and geometric isomerism of neoxanthin in oxygenic phototrophs: 9′-cis, a sole molecular form.Crossref | GoogleScholarGoogle Scholar |
Tellez P, Rojas E, Bael SV (2016) Red coloration in young tropical leaves associated with reduced fungal pathogen damage. Biotropica 48, 150–153.
| Red coloration in young tropical leaves associated with reduced fungal pathogen damage.Crossref | GoogleScholarGoogle Scholar |
Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnology Letters 30, 967–977.
| Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress.Crossref | GoogleScholarGoogle Scholar | 18227974PubMed |
Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiology 153, 895–905.
| Lignin biosynthesis and structure.Crossref | GoogleScholarGoogle Scholar | 20472751PubMed |
Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist 195, 306–320.
| Opportunities for improving phosphorus-use efficiency in crop plants.Crossref | GoogleScholarGoogle Scholar | 22691045PubMed |
Vrede T, Dobberfuhl DR, Kooijman SALM, Elser JJ (2004) Fundamental connections among organism C : N : P stoichiometry, macromolecular composition, and growth. Ecology 85, 1217–1229.
| Fundamental connections among organism C : N : P stoichiometry, macromolecular composition, and growth.Crossref | GoogleScholarGoogle Scholar |
Wang K, Tu W, Liu C, Rao Y, Gao Z, Yang C (2017) 9-cis-Neoxanthin in light harvesting complexes of photosystem II regulates the binding of violaxanthin and xanthophyll cycle. Plant Physiology 174, 86–96.
| 9-cis-Neoxanthin in light harvesting complexes of photosystem II regulates the binding of violaxanthin and xanthophyll cycle.Crossref | GoogleScholarGoogle Scholar | 28320865PubMed |
Woodall GS, Dodd IC, Stewart GR (1998) Contrasting leaf development within the genus Syzygium. Journal of Experimental Botany 49, 79–87.
| Contrasting leaf development within the genus Syzygium.Crossref | GoogleScholarGoogle Scholar |
Wrolstad RE, Durst RW, Lee J (2005) Tracking color and pigment changes in anthocyanin products. Trends in Food Science & Technology 16, 423–428.
| Tracking color and pigment changes in anthocyanin products.Crossref | GoogleScholarGoogle Scholar |
Yan Z, Li P, Chen Y, Han W, Fang J (2016) Nutrient allocation strategies of woody plants: an approach from the scaling of nitrogen and phosphorus between twig stems and leaves. Scientific Reports 6, 20099
| Nutrient allocation strategies of woody plants: an approach from the scaling of nitrogen and phosphorus between twig stems and leaves.Crossref | GoogleScholarGoogle Scholar | 26848020PubMed |
Yruela I (2005) Copper in plants. Brazilian Journal of Plant Physiology 17, 145–156.
| Copper in plants.Crossref | GoogleScholarGoogle Scholar |
Zasoski RJ, Burau RG (1977) A rapid nitric‐perchloric acid digestion method for multi‐element tissue analysis. Communications in Soil Science and Plant Analysis 8, 425–436.
| A rapid nitric‐perchloric acid digestion method for multi‐element tissue analysis.Crossref | GoogleScholarGoogle Scholar |
