Efficient phloem remobilization of Zn protects apple trees during the early stages of Zn deficiency
Abstract
Apple trees are extensively cultivated worldwide but are often affected by zinc (Zn) deficiency. Limited knowledge regarding Zn remobilization within fruit crops has hampered the development of efficient strategies for providing adequate amounts of Zn. In the present study, Zn distribution and remobilization were compared among apple trees cultivated under different Zn conditions. Without Zn application, plants showed visible symptoms of Zn deficiency at the shoot tips after 1 year but appeared to grow normally during the first 6 months (early stage of Zn deficiency). Compared with apple plants under sufficient Zn treatment, plants suffering from early-stage Zn deficiency showed preferential Zn distribution to young leaves and higher Zn levels in phloem, demonstrating that hidden Zn deficiency triggers a highly efficient remobilization of Zn in this species. The in vivo Zn-nicotianamine complex in phloem tissues, combined with the significant enhanced expression of MdNAS3 and MdYSL6 , suggested a positive role for nicotianamine in the phloem remobilization of Zn. These results strongly suggest that a proportion of Zn in the old leaves of apple trees can be efficiently remobilized by phloem transport to the shoot tips, partially in the form of Zn-nicotianamine, thus protecting apple trees against the early stages ofmore »
- Authors:
-
- Zhejiang Univ., Hangzhou (China)
- Univ. of California, Davis, CA (United States)
- SLAC National Accelerator Lab., Menlo Park, CA (United States)
- Publication Date:
- Research Org.:
- SLAC National Accelerator Lab., Menlo Park, CA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1637927
- Grant/Contract Number:
- AC02-76SF00515; 31471939
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Plant, Cell and Environment
- Additional Journal Information:
- Journal Volume: 42; Journal Issue: 12; Journal ID: ISSN 0140-7791
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; apple plants; distribution; fruit crops; micro X‐ray fluorescence; nicotianamine; phloem; remobilization; speciation; zinc; zinc deficiency
Citation Formats
Xie, Ruohan, Zhao, Jianqi, Lu, Lingli, Ge, Jun, Brown, Patrick H., Wei, Shuai, Wang, Runze, Qiao, Yabei, Webb, Samuel M., and Tian, Shengke. Efficient phloem remobilization of Zn protects apple trees during the early stages of Zn deficiency. United States: N. p., 2019.
Web. doi:10.1111/pce.13621.
Xie, Ruohan, Zhao, Jianqi, Lu, Lingli, Ge, Jun, Brown, Patrick H., Wei, Shuai, Wang, Runze, Qiao, Yabei, Webb, Samuel M., & Tian, Shengke. Efficient phloem remobilization of Zn protects apple trees during the early stages of Zn deficiency. United States. https://doi.org/10.1111/pce.13621
Xie, Ruohan, Zhao, Jianqi, Lu, Lingli, Ge, Jun, Brown, Patrick H., Wei, Shuai, Wang, Runze, Qiao, Yabei, Webb, Samuel M., and Tian, Shengke. Sat .
"Efficient phloem remobilization of Zn protects apple trees during the early stages of Zn deficiency". United States. https://doi.org/10.1111/pce.13621. https://www.osti.gov/servlets/purl/1637927.
@article{osti_1637927,
title = {Efficient phloem remobilization of Zn protects apple trees during the early stages of Zn deficiency},
author = {Xie, Ruohan and Zhao, Jianqi and Lu, Lingli and Ge, Jun and Brown, Patrick H. and Wei, Shuai and Wang, Runze and Qiao, Yabei and Webb, Samuel M. and Tian, Shengke},
abstractNote = {Apple trees are extensively cultivated worldwide but are often affected by zinc (Zn) deficiency. Limited knowledge regarding Zn remobilization within fruit crops has hampered the development of efficient strategies for providing adequate amounts of Zn. In the present study, Zn distribution and remobilization were compared among apple trees cultivated under different Zn conditions. Without Zn application, plants showed visible symptoms of Zn deficiency at the shoot tips after 1 year but appeared to grow normally during the first 6 months (early stage of Zn deficiency). Compared with apple plants under sufficient Zn treatment, plants suffering from early-stage Zn deficiency showed preferential Zn distribution to young leaves and higher Zn levels in phloem, demonstrating that hidden Zn deficiency triggers a highly efficient remobilization of Zn in this species. The in vivo Zn-nicotianamine complex in phloem tissues, combined with the significant enhanced expression of MdNAS3 and MdYSL6 , suggested a positive role for nicotianamine in the phloem remobilization of Zn. These results strongly suggest that a proportion of Zn in the old leaves of apple trees can be efficiently remobilized by phloem transport to the shoot tips, partially in the form of Zn-nicotianamine, thus protecting apple trees against the early stages of Zn deficiency.},
doi = {10.1111/pce.13621},
journal = {Plant, Cell and Environment},
number = 12,
volume = 42,
place = {United States},
year = {2019},
month = {7}
}
Web of Science
Figures / Tables:

Works referenced in this record:
Synchrotron-based techniques for plant and soil science: opportunities, challenges and future perspectives
journal, January 2009
- Lombi, Enzo; Susini, Jean
- Plant and Soil, Vol. 320, Issue 1-2
Zinc Mobility in Wheat: Uptake and Distribution of Zinc Applied to Leaves or Roots
journal, March 2001
- Haslett, B.
- Annals of Botany, Vol. 87, Issue 3
The zinc homeostasis network of land plants
journal, September 2012
- Sinclair, Scott Aleksander; Krämer, Ute
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1823, Issue 9
Zinc Efficiency Is Correlated with Enhanced Expression and Activity of Zinc-Requiring Enzymes in Wheat
journal, January 2003
- Hacisalihoglu, Gökhan; Hart, Jonathan J.; Wang, Yi-Hong
- Plant Physiology, Vol. 131, Issue 2
Comparative movement of labelled nitrogen and zinc in 1-year-old peach [ Prunus persica (L.) Batsch] trees following late-season foliar application
journal, January 2006
- Sanchez, E. E.; Weinbaum, S. A.; Johnson, R. S.
- The Journal of Horticultural Science and Biotechnology, Vol. 81, Issue 5
Spatial Imaging and Speciation of Lead in the Accumulator Plant Sedum alfredii by Microscopically Focused Synchrotron X-ray Investigation
journal, August 2010
- Tian, Shengke; Lu, Lingli; Yang, Xiaoe
- Environmental Science & Technology, Vol. 44, Issue 15
Seasonal changes in nutrient concentrations of navel orange fruit
journal, April 2000
- Storey, R.; Treeby, M. T.
- Scientia Horticulturae, Vol. 84, Issue 1-2
Impact of Contract Farming on Income: Linking Small Farmers, Packers, and Supermarkets in China
journal, November 2009
- Miyata, Sachiko; Minot, Nicholas; Hu, Dinghuan
- World Development, Vol. 37, Issue 11
Moving micronutrients from the soil to the seeds: Genes and physiological processes from a biofortification perspective
journal, April 2011
- Waters, Brian M.; Sankaran, Renuka P.
- Plant Science, Vol. 180, Issue 4
Zinc Nutrition of Fruit Crops
journal, January 2002
- Swietlik, Dariusz
- HortTechnology, Vol. 12, Issue 1
Zinc in plants
journal, March 2007
- Broadley, Martin R.; White, Philip J.; Hammond, John P.
- New Phytologist, Vol. 173, Issue 4
Enrichment of cereal grains with zinc: Agronomic or genetic biofortification?
journal, November 2007
- Cakmak, Ismail
- Plant and Soil, Vol. 302, Issue 1-2
Internal remobilization of carbohydrates, lipids, nitrogen and phosphorus in the Mediterranean evergreen oak Quercus ilex
journal, January 2001
- Cherbuy, B.; Joffre, R.; Gillon, D.
- Tree Physiology, Vol. 21, Issue 1
Placing metal micronutrients in context: transport and distribution in plants
journal, June 2009
- Puig, Sergi; Peñarrubia, Lola
- Current Opinion in Plant Biology, Vol. 12, Issue 3
Imaging element distribution and speciation in plant cells
journal, March 2014
- Zhao, Fang-Jie; Moore, Katie L.; Lombi, Enzo
- Trends in Plant Science, Vol. 19, Issue 3
Plant nutrition for sustainable development and global health
journal, April 2010
- White, P. J.; Brown, P. H.
- Annals of Botany, Vol. 105, Issue 7
Biofortification of crops with seven mineral elements often lacking in human diets - iron, zinc, copper, calcium, magnesium, selenium and iodine: Research review
journal, January 2009
- White, Philip J.; Broadley, Martin R.
- New Phytologist, Vol. 182, Issue 1
Morphology, photosynthesis, and internal structure alterations in field apple leaves under hidden and acute zinc deficiency
journal, September 2015
- Fu, Chunxia; Li, Ming; Zhang, Yong
- Scientia Horticulturae, Vol. 193
Zinc Application Effects on Yield and Seed Oil Content of Sunflower Grown on a Saline Calcareous Soil
journal, October 2006
- Mirzapour, M. H.; Khoshgoftar, A. H.
- Journal of Plant Nutrition, Vol. 29, Issue 10
A long way ahead: understanding and engineering plant metal accumulation
journal, July 2002
- Clemens, Stephan; Palmgren, Michael G.; Krämer, Ute
- Trends in Plant Science, Vol. 7, Issue 7
Zinc compartmentation in root, transport into xylem, and absorption into leaf cells in the hyperaccumulating species of Sedum alfredii Hance
journal, December 2005
- Yang, Xiaoe; Li, Tingqiang; Yang, Juncheng
- Planta, Vol. 224, Issue 1
Relationships between phenology and the remobilization of nitrogen, phosphorus and potassium in branches of eight Mediterranean evergreens
journal, June 2005
- Milla, R.; Castro-Díez, P.; Maestro-Martínez, M.
- New Phytologist, Vol. 168, Issue 1
Elemental and Chemically Specific X-ray Fluorescence Imaging of Biological Systems
journal, January 2014
- Pushie, M. Jake; Pickering, Ingrid J.; Korbas, Malgorzata
- Chemical Reviews, Vol. 114, Issue 17
Cellular Sequestration of Cadmium in the Hyperaccumulator Plant Species Sedum alfredii
journal, October 2011
- Tian, Shengke; Lu, Lingli; Labavitch, John
- Plant Physiology, Vol. 157, Issue 4
SIXPack a Graphical User Interface for XAS Analysis Using IFEFFIT
journal, January 2005
- Webb, S. M.
- Physica Scripta
From plant surface to plant metabolism: the uncertain fate of foliar-applied nutrients
journal, January 2013
- Fernández, Victoria; Brown, Patrick H.
- Frontiers in Plant Science, Vol. 4
Micronutrient Constraints to Crop Production in Soils with Mediterranean-type Characteristics: A Review
journal, December 2004
- Rashid, A.; Ryan, J.
- Journal of Plant Nutrition, Vol. 27, Issue 6
Role of sulfur assimilation pathway in cadmium hyperaccumulation by Sedum alfredii Hance
journal, February 2014
- Liang, Jun; Shohag, M. J. I.; Yang, Xiaoe
- Ecotoxicology and Environmental Safety, Vol. 100
Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters
journal, October 2008
- Curie, Catherine; Cassin, Gaëlle; Couch, Daniel
- Annals of Botany, Vol. 103, Issue 1
The domestication and evolutionary ecology of apples
journal, February 2014
- Cornille, Amandine; Giraud, Tatiana; Smulders, Marinus J. M.
- Trends in Genetics, Vol. 30, Issue 2
Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data
journal, February 2009
- Ruijter, J. M.; Ramakers, C.; Hoogaars, W. M. H.
- Nucleic Acids Research, Vol. 37, Issue 6
Efficient xylem transport and phloem remobilization of Zn in the hyperaccumulator plant species Sedum alfredii
journal, February 2013
- Lu, Lingli; Tian, Shengke; Zhang, Jie
- New Phytologist, Vol. 198, Issue 3
In situ analysis of foliar zinc absorption and short-distance movement in fresh and hydrated leaves of tomato and citrus using synchrotron-based X-ray fluorescence microscopy
journal, November 2014
- Du, Yumei; Kopittke, Peter M.; Noller, Barry N.
- Annals of Botany, Vol. 115, Issue 1
Boron in Plant Biology
journal, March 2002
- Brown, P. H.; Bellaloui, N.; Wimmer, M. A.
- Plant Biology, Vol. 4, Issue 2
Zinc as a Nutrient for Plants
journal, June 1937
- Chandler, W. H.
- Botanical Gazette, Vol. 98, Issue 4
Distribution and Transport of Foliar Applied Zinc in Pistachio
journal, July 1999
- Zhang, Qinglong; Brown, Patrick H.
- Journal of the American Society for Horticultural Science, Vol. 124, Issue 4
Translocation of nitrogen in the xylem of field-grown cherry and poplar trees during remobilization
journal, April 2006
- Millard, P.; Wendler, R.; Grassi, G.
- Tree Physiology, Vol. 26, Issue 4
Zinc biofortification of cereals: problems and solutions
journal, September 2008
- Palmgren, Michael G.; Clemens, Stephan; Williams, Lorraine E.
- Trends in Plant Science, Vol. 13, Issue 9
Spatial imaging of Zn and other elements in Huanglongbing-affected grapefruit by synchrotron-based micro X-ray fluorescence investigation
journal, January 2014
- Tian, Shengke; Lu, Lingli; Labavitch, John M.
- Journal of Experimental Botany, Vol. 65, Issue 4
Soil factors associated with zinc deficiency in crops and humans
journal, March 2009
- Alloway, B. J.
- Environmental Geochemistry and Health, Vol. 31, Issue 5
Biofortification-A Sustainable Agricultural Strategy for Reducing Micronutrient Malnutrition in the Global South
journal, March 2010
- Bouis, Howarth E.; Welch, Ross M.
- Crop Science, Vol. 50
Figures / Tables found in this record: