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PMID: 30535321 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Overexpression of rice aquaporin OsPIP1;2 improves yield by enhancing mesophyll CO2 conductance and phloem sucrose transport.

Journal of experimental botany ·Vol. 70 ·No. 2 ·2019-00-07 ·Pages 671-681

Xu F, Wang K, Yuan W, Xu W, Shuang L, Kronzucker HJ, Chen G, Miao R, Zhang M, Ding M, Xiao L, Kai L, Zhang J, Zhu Y

Abstract

Aquaporins are involved in CO2 transport from the leaf intercellular air space to the chloroplast, which contributes to CO2 assimilation. However, the mechanism of CO2 transport by rice (Oryza sativa L.) aquaporins is unknown. Here, we investigated the function of the aquaporin OsPIP1;2 in CO2 diffusion-associated photosynthesis and phloem sucrose transport. Moreover, the grain yield of rice lines overexpressing OsPIP1;2 was determined. OsPIP1;2 was localized to the plasma membrane and the relative expression of OsPIP1;2 was approximately 5-fold higher in leaves in the presence of an elevated CO2 concentration. Overexpression of OsPIP1;2 increased mesophyll conductance by approximately 150% compared with wild-type (WT) rice. The OsPIP1;2-overexpressing lines had higher biomass than the WT, possibly due to increased phloem sucrose transport. In addition, the grain yield of OsPIP1;2-overexpressing lines was approximately 25% higher than that of the WT in three-season field experiments, due to the increased numbers of effective tillers and spikelets per panicle. Our results suggest that OsPIP1;2 modulates rice growth and grain yield by facilitating leaf CO2 diffusion, which increases both the net CO2 assimilation rate and sucrose transport.

MeSH Terms
Aquaporins/metabolism Biomass Carbon Dioxide/metabolism Edible Grain/growth & development Mesophyll Cells/metabolism Oryza/growth & development,metabolism Phloem/metabolism Photosynthesis Sucrose/metabolism
Chemicals
Aquaporins Carbon Dioxide Sucrose
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Xu Feiyun
Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, College of Resources and Environmental Science, Nanjing Agricultural University, Nanjing, China. | College of Life Sciences and Joint International Research Laboratory of Water and Nutrient in Crops, Fujian Agriculture and Forestry University, Fuzhou, China.
Wang Ke
College of Life Sciences and Joint International Research Laboratory of Water and Nutrient in Crops, Fujian Agriculture and Forestry University, Fuzhou, China.
Yuan Wei
College of Life Sciences and Joint International Research Laboratory of Water and Nutrient in Crops, Fujian Agriculture and Forestry University, Fuzhou, China.
Xu Weifeng
College of Life Sciences and Joint International Research Laboratory of Water and Nutrient in Crops, Fujian Agriculture and Forestry University, Fuzhou, China.
Shuang Liu
Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, College of Resources and Environmental Science, Nanjing Agricultural University, Nanjing, China.
Kronzucker Herbert J
School of Agriculture and Food, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, VIC, Australia.
Chen Guanglei
Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, College of Resources and Environmental Science, Nanjing Agricultural University, Nanjing, China.
Miao Rui
College of Life Sciences and Joint International Research Laboratory of Water and Nutrient in Crops, Fujian Agriculture and Forestry University, Fuzhou, China.
Zhang Maoxing
Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, College of Resources and Environmental Science, Nanjing Agricultural University, Nanjing, China.
Ding Ming
Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, College of Resources and Environmental Science, Nanjing Agricultural University, Nanjing, China.
Xiao Liang
Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, College of Resources and Environmental Science, Nanjing Agricultural University, Nanjing, China.
Kai Lei
The Key Laboratory of Biotechnology for Medicinal Plants of Jiangsu Province, Jiangsu Key Laboratory of Phylogenomics and Comparative Genomics, School of Life Sciences, Jiangsu Normal University, Xuzhou, China.
Zhang Jianhua
Department of Biology, Hong Kong Baptist University, and the State Key Laboratory of Agrobiotechnology, Chinese University of Hong Kong, Hong Kong, China.
Zhu Yiyong
Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, College of Resources and Environmental Science, Nanjing Agricultural University, Nanjing, China.
References (43)
43 references, click to expand
  1. Sucrose is a signal molecule in assimilate partitioning.
    Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4784-8 PMID: 9539816
  2. Coordination of Leaf Photosynthesis, Transpiration, and Structural Traits in Rice and Wild Relatives (Genus Oryza).
    Plant Physiol. 2013 Jul;162(3):1632-51 PMID: 23669746
  3. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2.
    New Phytol. 2005 Feb;165(2):351-71 PMID: 15720649
  4. Identification of actively filling sucrose sinks.
    Plant Physiol. 1989 Apr;89(4):1117-21 PMID: 16666673
  5. Monitoring plant and soil water status: established and novel methods revisited and their relevance to studies of drought tolerance.
    J Exp Bot. 2007;58(2):119-30 PMID: 16980592
  6. A node-based switch for preferential distribution of manganese in rice.
    Nat Commun. 2013;4:2442 PMID: 24048172
  7. Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low-nitrogen conditions.
    Plant Biotechnol J. 2011 Oct;9(8):826-37 PMID: 21624033
  8. Overexpression of the barley aquaporin HvPIP2;1 increases internal CO(2) conductance and CO(2) assimilation in the leaves of transgenic rice plants.
    Plant Cell Physiol. 2004 May;45(5):521-9 PMID: 15169933
  9. The effect of exogenous abscisic acid on stomatal development, stomatal mechanics, and leaf gas exchange in Tradescantia virginiana.
    Plant Physiol. 2001 Feb;125(2):935-42 PMID: 11161050
  10. Origin of sucrose metabolism in higher plants: when, how and why?
    Trends Plant Sci. 2003 Feb;8(2):63-9 PMID: 12597872
  11. Mesophyll conductance to CO2: current knowledge and future prospects.
    Plant Cell Environ. 2008 May;31(5):602-21 PMID: 17996013
  12. Enhancement of Phloem exudation from cut petioles by chelating agents.
    Plant Physiol. 1974 Jan;53(1):96-103 PMID: 16658661
  13. Fitting photosynthetic carbon dioxide response curves for C(3) leaves.
    Plant Cell Environ. 2007 Sep;30(9):1035-40 PMID: 17661745
  14. Resistances along the CO2 diffusion pathway inside leaves.
    J Exp Bot. 2009;60(8):2235-48 PMID: 19395390
  15. The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO₂ transport facilitator.
    Plant J. 2011 Sep;67(5):795-804 PMID: 21564354
  16. Standards for plant synthetic biology: a common syntax for exchange of DNA parts.
    New Phytol. 2015 Oct;208(1):13-9 PMID: 26171760
  17. Seasonal time-course of gradients of photosynthetic capacity and mesophyll conductance to CO2 across a beech (Fagus sylvatica L.) canopy.
    J Exp Bot. 2009;60(8):2407-18 PMID: 19457983
  18. Knockdown of a rice stelar nitrate transporter alters long-distance translocation but not root influx.
    Plant Physiol. 2012 Dec;160(4):2052-63 PMID: 23093362
  19. CO2 transport by PIP2 aquaporins of barley.
    Plant Cell Physiol. 2014 Feb;55(2):251-7 PMID: 24406630
  20. Differential tissue-specific expression of NtAQP1 in Arabidopsis thaliana reveals a role for this protein in stomatal and mesophyll conductance of CO₂ under standard and salt-stress conditions.
    Planta. 2014 Feb;239(2):357-66 PMID: 24170337
  21. Increased leaf photosynthesis caused by elevated stomatal conductance in a rice mutant deficient in SLAC1, a guard cell anion channel protein.
    J Exp Bot. 2012 Sep;63(15):5635-44 PMID: 22915747
  22. Overexpression of plasma membrane H+-ATPase in guard cells promotes light-induced stomatal opening and enhances plant growth.
    Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):533-8 PMID: 24367097
  23. Plasma membrane protein OsMCA1 is involved in regulation of hypo-osmotic shock-induced Ca2+ influx and modulates generation of reactive oxygen species in cultured rice cells.
    BMC Plant Biol. 2012 Jan 23;12:11 PMID: 22264357
  24. Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation.
    Plant J. 2009 Mar;57(5):798-809 PMID: 18980647
  25. Rapid responses of mesophyll conductance to changes of CO2 concentration, temperature and irradiance are affected by N supplements in rice.
    Plant Cell Environ. 2015 Dec;38(12):2541-50 PMID: 25923314
  26. Using combined measurements of gas exchange and chlorophyll fluorescence to estimate parameters of a biochemical C photosynthesis model: a critical appraisal and a new integrated approach applied to leaves in a wheat (Triticum aestivum) canopy.
    Plant Cell Environ. 2009 May;32(5):448-64 PMID: 19183300
  27. Identification of 33 rice aquaporin genes and analysis of their expression and function.
    Plant Cell Physiol. 2005 Sep;46(9):1568-77 PMID: 16033806
  28. Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment.
    Cell Res. 2006 Jul;16(7):651-60 PMID: 16773042
  29. Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability.
    Plant Cell. 2008 Mar;20(3):648-57 PMID: 18349152
  30. Theoretical Considerations when Estimating the Mesophyll Conductance to CO(2) Flux by Analysis of the Response of Photosynthesis to CO(2).
    Plant Physiol. 1992 Apr;98(4):1429-36 PMID: 16668811
  31. Model-data synthesis for the next generation of forest free-air CO2 enrichment (FACE) experiments.
    New Phytol. 2016 Jan;209(1):17-28 PMID: 26249015
  32. Photosynthesis-dependent and -independent responses of stomata to blue, red and green monochromatic light: differences between the normally oriented and inverted leaves of sunflower.
    Plant Cell Physiol. 2011 Mar;52(3):479-89 PMID: 21257606
  33. Coupling of CO2 and ice sheet stability over major climate transitions of the last 20 million years.
    Science. 2009 Dec 4;326(5958):1394-7 PMID: 19815724
  34. The phosphate transporter gene OsPht1;8 is involved in phosphate homeostasis in rice.
    Plant Physiol. 2011 Jul;156(3):1164-75 PMID: 21502185
  35. Crop responses to elevated CO2 and interactions with H2O, N, and temperature.
    Curr Opin Plant Biol. 2016 Jun;31:36-43 PMID: 27043481
  36. Adaptation of plasma membrane H(+)-ATPase of rice roots to low pH as related to ammonium nutrition.
    Plant Cell Environ. 2009 Oct;32(10):1428-40 PMID: 19558410
  37. Aquaporin plays an important role in mediating chloroplastic CO2 concentration under high-N supply in rice (Oryza sativa) plants.
    Physiol Plant. 2016 Feb;156(2):215-226 PMID: 26382720
  38. The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions.
    Nature. 2003 Oct 16;425(6959):734-7 PMID: 14520414
  39. Structural mechanism of plant aquaporin gating.
    Nature. 2006 Feb 9;439(7077):688-94 PMID: 16340961
  40. Analysis of leakage in IRGA's leaf chambers of open gas exchange systems: quantification and its effects in photosynthesis parameterization.
    J Exp Bot. 2007;58(6):1533-43 PMID: 17339650
  41. Enhancing C3 photosynthesis: an outlook on feasible interventions for crop improvement.
    Plant Biotechnol J. 2014 Dec;12(9):1217-30 PMID: 25196090
  42. Low stomatal and internal conductance to CO2 versus Rubisco deactivation as determinants of the photosynthetic decline of ageing evergreen leaves.
    Plant Cell Environ. 2006 Dec;29(12):2168-84 PMID: 17081250
  43. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency.
    Plant Physiol. 2014 Apr;164(4):1556-70 PMID: 24578506
Article Info
Journal
Journal of experimental botany
Abbr.
J Exp Bot
ISSN
1460-2431
Published
2019-00-07
Pages
671-681
Language
English
Region
England
NLM ID
9882906
PMCID
PMC6322580
Subset
IM
Corrections
ErratumIn
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