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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Global convergence in the balance between leaf water supply and demand across vascular land plants

Yin Wen https://orcid.org/0000-0002-0262-8876 A B , Wan-li Zhao C D and Kun-fang Cao A B E
+ Author Affiliations
- Author Affiliations

A Plant Ecophysiology and Evolution Group, State Key Laboratory for Conservation and Utilisation of Subtropical Agro-Bioresources, Guangxi University, Nanning, Guangxi 530004, China.

B Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, Guangxi 530004, China.

C Shandong Provincial Key Laboratory of Eco-Environmental Science for Yellow River Delta, Binzhou University, Binzhou, Shandong 256600, China.

D Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China.

E Corresponding author. Email: kunfangcao@gxu.edu.cn

Functional Plant Biology 47(10) 904-911 https://doi.org/10.1071/FP19101
Submitted: 13 April 2019  Accepted: 16 April 2020   Published: 8 July 2020

Abstract

Coordination between the density of veins (water supply) and stomata (demand for water) has been found in the leaves of modern angiosperms and also in ferns. This suggests that this coordinated development is not a unique adaptation of derived angiosperms that enables their high productivity. To test this, we compiled leaf vein and stomatal density data from 520 land vascular plant species including derived angiosperms, basal angiosperms, gymnosperms and ferns. We found global coordination across vascular land plants, although the relationships were not significant in gymnosperms and vessel-less angiosperms. By comparing the evolution of xylem conduit elements with variation in the density of veins and stomata and theoretical stomatal conductance among plant lineages, we found that the physiological advantage of modern angiosperms is associated with the emergence of xylem with low intraconduit resistance and leaves with high vein and stomata densities. Thus our results indicate two major events associated with surges in xylem hydraulic capacity in angiosperms: (1) the origin of vessels and (2) the emergence of vessels with simple perforation plates, which diminished physical limitations on stomatal conductance. These evolutionary innovations may have enabled derived angiosperms to be more productive and adaptive to the changing climate.

Additional keywords: carbon uptake, hydraulic conductance, leaf photosynthetic rate, transpiration.


References

Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society B 276, 1771–1776.
Angiosperm leaf vein evolution was physiologically and environmentally transformative.Crossref | GoogleScholarGoogle Scholar | 19324775PubMed |

Brodribb TJ, Jordan GJ (2011) Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees. New Phytologist 192, 437–448.
Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees.Crossref | GoogleScholarGoogle Scholar | 21679190PubMed |

Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144, 1890–1898.
Leaf maximum photosynthetic rate and venation are linked by hydraulics.Crossref | GoogleScholarGoogle Scholar | 17556506PubMed |

Brodribb TJ, Feild TS, Sack L (2010) Viewing leaf structure and evolution from a hydraulic perspective. Functional Plant Biology 37, 488–498.
Viewing leaf structure and evolution from a hydraulic perspective.Crossref | GoogleScholarGoogle Scholar |

Brodribb TJ, Jordan GJ, Carpenter RJ (2013) Unified changes in cell size permit coordinated leaf evolution. New Phytologist 199, 559–570.
Unified changes in cell size permit coordinated leaf evolution.Crossref | GoogleScholarGoogle Scholar | 23647069PubMed |

Brodribb TJ, McAdam S A M, Carins Murphy MR (2017) Xylem and stomata, coordinated through time and space. Plant, Cell & Environment 40, 872–880.
Xylem and stomata, coordinated through time and space.Crossref | GoogleScholarGoogle Scholar |

Carins Murphy MR, Jordan GJ, Brodribb TJ (2012) Differential leaf expansion can enable hydraulic acclimation to sun and shade. Plant, Cell & Environment 35, 1407–1418.
Differential leaf expansion can enable hydraulic acclimation to sun and shade.Crossref | GoogleScholarGoogle Scholar |

Carins Murphy MR, Jordan GJ, Brodribb TJ (2016) Cell expansion not cell differentiation predominantly co-ordinates veins and stomata within and among herbs and woody angiosperms grown under sun and shade. Annals of Botany 118, 1127–1138.
Cell expansion not cell differentiation predominantly co-ordinates veins and stomata within and among herbs and woody angiosperms grown under sun and shade.Crossref | GoogleScholarGoogle Scholar | 27578763PubMed |

Carins Murphy MR, Jordan GJ, Brodribb TJ (2017) Ferns are less dependent on passive dilution by cell expansion to coordinate leaf vein and stomatal spacing than angiosperms. PLoS One 12, e0185648
Ferns are less dependent on passive dilution by cell expansion to coordinate leaf vein and stomatal spacing than angiosperms.Crossref | GoogleScholarGoogle Scholar | 28953931PubMed |

Carlquist S, Schneider EL (2007) Tracheary elements in ferns: new techniques, observations, and concepts. American Fern Journal 97, 199–211.
Tracheary elements in ferns: new techniques, observations, and concepts.Crossref | GoogleScholarGoogle Scholar |

Christman MA, Sperry JS (2010) Single-vessel flow measurements indicate scalariform perforation plates confer higher flow resistance than previously estimated. Plant, Cell & Environment 33, 431–443.
Single-vessel flow measurements indicate scalariform perforation plates confer higher flow resistance than previously estimated.Crossref | GoogleScholarGoogle Scholar |

de Boer HJ, Eppinga MB, Wassen MJ, Dekker SC (2012) A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution. Nature Communications 3, 1221
A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution.Crossref | GoogleScholarGoogle Scholar | 23187621PubMed |

de Boer HJ, Price CA, Wagner-Cremer F, Dekker SC, Franks PJ, Veneklaas EJ (2016) Optimal allocation of leaf epidermal area for gas exchange. New Phytologist 210, 1219–1228.
Optimal allocation of leaf epidermal area for gas exchange.Crossref | GoogleScholarGoogle Scholar | 26991124PubMed |

Ding L-Z, Chen Y-J, Zhang J-L (2014) Leaf traits and their associations among liana species in tropical rainforest. Zhiwu Kexue Xuebao 32, 362–370.

Feild TS, Brodribb TJ (2013) Hydraulic tuning of vein cell microstructure in the evolution of angiosperm venation networks. New Phytologist 199, 720–726.
Hydraulic tuning of vein cell microstructure in the evolution of angiosperm venation networks.Crossref | GoogleScholarGoogle Scholar | 23668223PubMed |

Feild TS, Wilson JP (2012) Evolutionary voyage of angiosperm vessel structure–function and its significance for early angiosperm success. International Journal of Plant Sciences 173, 596–609.
Evolutionary voyage of angiosperm vessel structure–function and its significance for early angiosperm success.Crossref | GoogleScholarGoogle Scholar |

Feild TS, Chatelet DS, Brodribb TJ (2009) Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms. Geobiology 7, 237–264.
Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms.Crossref | GoogleScholarGoogle Scholar | 19260972PubMed |

Feild TS, Brodribb TJ, Iglesias A, Chatelet DS, Baresch A, Upchurch GR, Gomez B, Mohr B A R, Coiffard C, Kvacek J, Jaramillo C (2011) Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences of the United States of America 108, 8363–8366.
Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution.Crossref | GoogleScholarGoogle Scholar | 21536892PubMed |

Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences of the United States of America 106, 10343–10347.
Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time.Crossref | GoogleScholarGoogle Scholar | 19506250PubMed |

Franks PJ, Royer DL, Beerling DJ, Van de Water PK, Cantrill DJ, Barbour MM, Berry JA (2014) New constraints on atmospheric CO2 concentration for the Phanerozoic. Geophysical Research Letters 41, 4685–4694.
New constraints on atmospheric CO2 concentration for the Phanerozoic.Crossref | GoogleScholarGoogle Scholar |

Jansen S, Nardini A (2014) From systematic to ecological wood anatomy and finally plant hydraulics: are we making progress in understanding xylem evolution? New Phytologist 203, 12–15.
From systematic to ecological wood anatomy and finally plant hydraulics: are we making progress in understanding xylem evolution?Crossref | GoogleScholarGoogle Scholar | 24807224PubMed |

McElwain JC, Yiotis C, Lawson T (2016) Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution. New Phytologist 209, 94–103.
Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution.Crossref | GoogleScholarGoogle Scholar | 26230251PubMed |

McKown AD, Cochard H, Sack L (2010) Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution. American Naturalist 175, 447–460.
Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution.Crossref | GoogleScholarGoogle Scholar | 20178410PubMed |

Sack L, Frole K (2006) Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87, 483–491.
Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees.Crossref | GoogleScholarGoogle Scholar | 16637372PubMed |

Sack L, Holbrook NM (2006) Leaf hydraulics. Annual Review of Plant Biology 57, 361–381.
Leaf hydraulics.Crossref | GoogleScholarGoogle Scholar | 16669766PubMed |

Sack L, Scoffoni C (2013) Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytologist 198, 983–1000.
Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future.Crossref | GoogleScholarGoogle Scholar | 23600478PubMed |

Sack L, Scoffoni C, Johnson DM, Buckley TN, Brodribb TJ (2015) The anatomical determinants of leaf hydraulic function. In ‘Functional and ecological xylem anatomy’. (Ed U. Hacke), pp. 255–271. (Springer International Publishing: Cham)

Schweingruber FH, Börner A, Schulze ED (2011) ‘Atlas of stem anatomy in herbs, shrubs and trees, Volume 1.’ (Springer-Verlag: Berlin Heidelberg)

Schweingruber FH, Börner A, Schulze ED (2013) ‘Atlas of stem anatomy in herbs, shrubs and trees, Volume 2.’ (Springer-Verlag: Berlin Heidelberg)

Scoffoni C, Chatelet DS, Pasquet-kok J, Rawls M, Donoghue MJ, Edwards EJ, Sack L (2016) Hydraulic basis for the evolution of photosynthetic productivity. Nature Plants 2, 16072
Hydraulic basis for the evolution of photosynthetic productivity.Crossref | GoogleScholarGoogle Scholar | 27255836PubMed |

Simonin KA, Roddy AB (2018) Genome downsizing, physiological novelty, and the global dominance of flowering plants. PLoS Biology 16, e2003706
Genome downsizing, physiological novelty, and the global dominance of flowering plants.Crossref | GoogleScholarGoogle Scholar | 29324757PubMed |

Trueba S, Delzon S, Isnard S, Lens F (2019) Similar hydraulic efficiency and safety across vesselless angiosperms and vessel-bearing species with scalariform perforation plates. Journal of Experimental Botany 70, 3227–3240.
Similar hydraulic efficiency and safety across vesselless angiosperms and vessel-bearing species with scalariform perforation plates.Crossref | GoogleScholarGoogle Scholar | 30921455PubMed |

Walls RL (2011) Angiosperm leaf vein patterns are linked to leaf functions in a global-scale data set. American Journal of Botany 98, 244–253.
Angiosperm leaf vein patterns are linked to leaf functions in a global-scale data set.Crossref | GoogleScholarGoogle Scholar | 21613113PubMed |

Zhang SB, Guan ZJ, Sun M, Zhang JJ, Cao KF, Hu H (2012) Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum, Orchidaceae. PLoS One 7, e40080
Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum, Orchidaceae.Crossref | GoogleScholarGoogle Scholar | 22792225PubMed |

Zhang SB, Sun M, Cao KF, Hu H, Zhang JL (2014a) Leaf photosynthetic rate of tropical ferns is evolutionarily linked to water transport capacity. PLoS One 9, e84682
Leaf photosynthetic rate of tropical ferns is evolutionarily linked to water transport capacity.Crossref | GoogleScholarGoogle Scholar | 24416265PubMed |

Zhang Y, Yang Shi J, Sun M, Cao K-F (2014b) Stomatal traits are evolutionarily associated with vein density in basal angiosperms. Zhiwu Kexue Xuebao 32, 320–328.

Zhang S-B, Dai Y, Hao G-Y, Li J-W, Fu X-W, Zhang J-L (2015a) Differentiation of water-related traits in terrestrial and epiphytic Cymbidium species. Frontiers in Plant Science 6, 260
Differentiation of water-related traits in terrestrial and epiphytic Cymbidium species.Crossref | GoogleScholarGoogle Scholar | 25954289PubMed |

Zhang YJ, Cao KF, Sack L, Li N, Wei XM, Goldstein G (2015b) Extending the generality of leaf economic design principles in the cycads, an ancient lineage. New Phytologist 206, 817–829.
Extending the generality of leaf economic design principles in the cycads, an ancient lineage.Crossref | GoogleScholarGoogle Scholar | 25622799PubMed |

Zhang FP, Murphy MR, Cardoso AA, Jordan GJ, Brodribb TJ (2018) Similar geometric rules govern the distribution of veins and stomata in petals, sepals and leaves. New Phytologist 219, 1224–1234.
Similar geometric rules govern the distribution of veins and stomata in petals, sepals and leaves.Crossref | GoogleScholarGoogle Scholar | 29761509PubMed |

Zhao WL, Chen YJ, Brodribb TJ, Cao KF (2016) Weak co-ordination between vein and stomatal densities in 105 angiosperm tree species along altitudinal gradients in Southwest China. Functional Plant Biology 43, 1126–1133.
Weak co-ordination between vein and stomatal densities in 105 angiosperm tree species along altitudinal gradients in Southwest China.Crossref | GoogleScholarGoogle Scholar | 32480532PubMed |

Zhao WL, Siddiq Z, Fu PL, Zhang JL, Cao KF (2017) Stable stomatal number per minor vein length indicates the coordination between leaf water supply and demand in three leguminous species. Scientific Reports 7, 2211–2221.
Stable stomatal number per minor vein length indicates the coordination between leaf water supply and demand in three leguminous species.Crossref | GoogleScholarGoogle Scholar | 28526823PubMed |

Zwieniecki MA, Boyce CK (2014) Evolution of a unique anatomical precision in angiosperm leaf venation lifts constraints on vascular plant ecology. Proceedings. Biological Sciences 281, 20132829
Evolution of a unique anatomical precision in angiosperm leaf venation lifts constraints on vascular plant ecology.Crossref | GoogleScholarGoogle Scholar | 24478301PubMed |