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

Drought resistance of cotton (Gossypium hirsutum) is promoted by early stomatal closure and leaf shedding

Ximeng Li https://orcid.org/0000-0002-7816-5441 A , Renee Smith A , Brendan Choat A and David T. Tissue https://orcid.org/0000-0002-8497-2047 A B
+ Author Affiliations
- Author Affiliations

A Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith, NSW 2751, Australia.

B Corresponding author. Email: D.Tissue@westernsydney.edu.au

Functional Plant Biology 47(2) 91-98 https://doi.org/10.1071/FP19093
Submitted: 5 April 2019  Accepted: 6 September 2019   Published: 12 December 2019

Abstract

Water relations have been well documented in tree species, but relatively little is known about the hydraulic characteristics of crops. Here, we report on the hydraulic strategy of cotton (Gossypium hirsutum L.). Leaf gas exchange and in vivo embolism formation were monitored simultaneously on plants that were dried down in situ under controlled environment conditions, and xylem vulnerability to embolism of leaves, stems and roots was measured using intact plants. Water potential inducing 50% embolised vessels (P50) in leaves was significantly higher (less negative) than P50 of stems and roots, suggesting that leaves were the most vulnerable organ to embolism. Furthermore, the water potential generating stomatal closure (Pgs) was higher than required to generate embolism formation, and complete stomatal closure always preceded the onset of embolism with declining soil water content. Although protracted drought resulted in massive leaf shedding, stem embolism remained minimal even after ~90% leaf area was lost. Overall, cotton maintained hydraulic integrity during long-term drought stress through early stomatal closure and leaf shedding, thus exhibiting a drought avoidance strategy. Given that water potentials triggering xylem embolism are uncommon under field conditions, cotton is unlikely to experience hydraulic dysfunction except under extreme climates. Results of this study provide physiological evidence for drought resistance in cotton with regard to hydraulics, and may provide guidance in developing irrigation schedules during periods of water shortage.

Additional keywords: hydraulic segmentation, leaf shedding, native embolism, stomatal regulation, water relation, xylem embolism.


References

Ackerson RC, Hebert RR (1981) Osmoregulation in cotton in response to water stress: I. Alterations in photosynthesis, leaf conductance, translocation, and ultrastructure. Plant Physiology 67, 484–488.
Osmoregulation in cotton in response to water stress: I. Alterations in photosynthesis, leaf conductance, translocation, and ultrastructure.Crossref | GoogleScholarGoogle Scholar | 16661699PubMed |

Alder N, Sperry J, Pockman W (1996) Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia 105, 293–301.
Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient.Crossref | GoogleScholarGoogle Scholar | 28307101PubMed |

Blackman CJ, Brodribb TJ, Jordan GJ (2009) Leaf hydraulics and drought stress: response, recovery and survivorship in four woody temperate plant species. Plant, Cell & Environment 32, 1584–1595.
Leaf hydraulics and drought stress: response, recovery and survivorship in four woody temperate plant species.Crossref | GoogleScholarGoogle Scholar |

Bourne AE, Creek D, Peters JM, Ellsworth DS, Choat B (2017) Species climate range influences hydraulic and stomatal traits in Eucalyptus species. Annals of Botany 120, 123–133.
Species climate range influences hydraulic and stomatal traits in Eucalyptus species.Crossref | GoogleScholarGoogle Scholar | 28369162PubMed |

Brodribb T, Feild T (2000) Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests. Plant, Cell & Environment 23, 1381–1388.
Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests.Crossref | GoogleScholarGoogle Scholar |

Brodribb TJ, Skelton RP, McAdam SA, Bienaimé D, Lucani CJ, Marmottant P (2016) Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytologist 209, 1403–1409.
Visual quantification of embolism reveals leaf vulnerability to hydraulic failure.Crossref | GoogleScholarGoogle Scholar | 26742653PubMed |

Brodribb TJ, Carriqui M, Delzon S, Lucani C (2017) Optical measurement of stem xylem vulnerability. Plant Physiology 174, 2054–2061.
Optical measurement of stem xylem vulnerability.Crossref | GoogleScholarGoogle Scholar | 28684434PubMed |

Broughton KJ, Smith RA, Duursma RA, Tan DK, Payton P, Bange MP, Tissue DT (2017) Warming alters the positive impact of elevated CO2 concentration on cotton growth and physiology during soil water deficit. Functional Plant Biology 44, 267–278.
Warming alters the positive impact of elevated CO2 concentration on cotton growth and physiology during soil water deficit.Crossref | GoogleScholarGoogle Scholar |

Charrier G, Delzon S, Domec JC, Zhang L, Delmas CE, Merlin I, Corso D, King A, Ojeda H, Ollat N (2018) Drought will not leave your glass empty: low risk of hydraulic failure revealed by long-term drought observations in world’s top wine regions. Science advances 4, eaao6969
Drought will not leave your glass empty: low risk of hydraulic failure revealed by long-term drought observations in world’s top wine regions.Crossref | GoogleScholarGoogle Scholar | 29404405PubMed |

Chastain DR, Snider JL, Collins GD, Perry CD, Whitaker J, Byrd SA (2014) Water deficit in field-grown Gossypium hirsutum primarily limits net photosynthesis by decreasing stomatal conductance, increasing photorespiration, and increasing the ratio of dark respiration to gross photosynthesis. Journal of Plant Physiology 171, 1576–1585.
Water deficit in field-grown Gossypium hirsutum primarily limits net photosynthesis by decreasing stomatal conductance, increasing photorespiration, and increasing the ratio of dark respiration to gross photosynthesis.Crossref | GoogleScholarGoogle Scholar | 25151126PubMed |

Choat B, Lahr EC, Melcher PJ, Zwieniecki MA, Holbrook NM (2005) The spatial pattern of air seeding thresholds in mature sugar maple trees. Plant, Cell & Environment 28, 1082–1089.
The spatial pattern of air seeding thresholds in mature sugar maple trees.Crossref | GoogleScholarGoogle Scholar |

Choat B, Drayton WM, Brodersen C, Matthews MA, Shackel KA, Wada H, McElrone AJ (2010) Measurement of vulnerability to water stress‐induced cavitation in grapevine: a comparison of four techniques applied to a long‐vesseled species. Plant, Cell & Environment 33, 1502–1512.
Measurement of vulnerability to water stress‐induced cavitation in grapevine: a comparison of four techniques applied to a long‐vesseled species.Crossref | GoogleScholarGoogle Scholar |

Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG (2012) Global convergence in the vulnerability of forests to drought. Nature 491, 752–755.
Global convergence in the vulnerability of forests to drought.Crossref | GoogleScholarGoogle Scholar | 23172141PubMed |

Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE (2018) Triggers of tree mortality under drought. Nature 558, 531–539.
Triggers of tree mortality under drought.Crossref | GoogleScholarGoogle Scholar | 29950621PubMed |

Cochard H, Delzon S (2013) Hydraulic failure and repair are not routine in trees. Annals of Forest Science 70, 659–661.
Hydraulic failure and repair are not routine in trees.Crossref | GoogleScholarGoogle Scholar |

Creek D, Blackman CJ, Brodribb TJ, Choat B, Tissue DT (2018) Coordination between leaf, stem, and root hydraulics and gas exchange in three arid‐zone angiosperms during severe drought and recovery. Plant, Cell & Environment 41, 2869–2881.
Coordination between leaf, stem, and root hydraulics and gas exchange in three arid‐zone angiosperms during severe drought and recovery.Crossref | GoogleScholarGoogle Scholar |

Cruiziat P, Cochard H, Améglio T (2002) Hydraulic architecture of trees: main concepts and results. Annals of Forest Science 59, 723–752.
Hydraulic architecture of trees: main concepts and results.Crossref | GoogleScholarGoogle Scholar |

Devi MJ, Reddy VRR (2018) Transpiration response of cotton to vapor pressure deficit and its relationship with stomatal traits. Frontiers in Plant Science 9, 1572
Transpiration response of cotton to vapor pressure deficit and its relationship with stomatal traits.Crossref | GoogleScholarGoogle Scholar | 30420866PubMed |

Duursma RA, Choat B (2017) fitplc: An R package to fit hydraulic vulnerability curves. The Journal of Plant Hydraulics 4, e002
fitplc: An R package to fit hydraulic vulnerability curves.Crossref | GoogleScholarGoogle Scholar |

Ghannoum O, Phillips NG, Conroy JP, Smith RA, Attard RD, Woodfield R, Logan BA, Lewis JD, Tissue DT (2009) Exposure to preindustrial, current and future atmospheric CO2 and temperature differentially affects growth and photosynthesis in Eucalyptus Global Change Biology 16, 303–319.
Exposure to preindustrial, current and future atmospheric CO2 and temperature differentially affects growth and photosynthesis in EucalyptusCrossref | GoogleScholarGoogle Scholar |

Gitz DC, Baker JT, Lascano RJ (2015) Relating xylem cavitation to gas exchange in cotton. American Journal of Plant Sciences 6, 1742–1751.
Relating xylem cavitation to gas exchange in cotton.Crossref | GoogleScholarGoogle Scholar |

Hochberg U, Windt CW, Ponomarenko A, Zhang Y-J, Gersony J, Rockwell FE, Holbrook NM (2017) Stomatal closure, basal leaf embolism and shedding protect the hydraulic integrity of grape stems. Plant Physiology 174, 764–775.
Stomatal closure, basal leaf embolism and shedding protect the hydraulic integrity of grape stems.Crossref | GoogleScholarGoogle Scholar | 28351909PubMed |

Johnson DM, Wortemann R, McCulloh KA, Jordan-Meille L, Ward E, Warren JM, Palmroth S, Domec JC (2016) A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species. Tree Physiology 36, 983–993.
A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species.Crossref | GoogleScholarGoogle Scholar | 27146334PubMed |

Klepsch M, Zhang Y, Kotowska MM, Lamarque LJ, Nolf M, Schuldt B, Torres-Ruiz JM, Qin DW, Choat B, Delzon S (2018) Is xylem of angiosperm leaves less resistant to embolism than branches? Insights from microCT, hydraulics, and anatomy. Journal of Experimental Botany 69, 5611–5623.
Is xylem of angiosperm leaves less resistant to embolism than branches? Insights from microCT, hydraulics, and anatomy.Crossref | GoogleScholarGoogle Scholar | 30184113PubMed |

Lauenroth W, Sala O, Milchunas D, Lathrop R (1987) Root dynamics of Bouteloua gracilis during short-term recovery from drought. Functional Ecology 1, 117–124.
Root dynamics of Bouteloua gracilis during short-term recovery from drought.Crossref | GoogleScholarGoogle Scholar |

Li Y, Sperry JS, Shao M (2009) Hydraulic conductance and vulnerability to cavitation in corn (Zea mays L.) hybrids of differing drought resistance. Environmental and Experimental Botany 66, 341–346.
Hydraulic conductance and vulnerability to cavitation in corn (Zea mays L.) hybrids of differing drought resistance.Crossref | GoogleScholarGoogle Scholar |

Li S, Feifel M, Karimi Z, Schuldt B, Choat B, Jansen S (2015) Leaf gas exchange performance and the lethal water potential of five European species during drought. Tree Physiology 36, 179–192.
Leaf gas exchange performance and the lethal water potential of five European species during drought.Crossref | GoogleScholarGoogle Scholar | 26614785PubMed |

Li X, Blackman CJ, Choat B, Duursma RA, Rymer PD, Medlyn BE, Tissue DT (2018) Tree hydraulic traits are coordinated and strongly linked to climate‐of‐origin across a rainfall gradient. Plant, Cell & Environment 41, 646–660.
Tree hydraulic traits are coordinated and strongly linked to climate‐of‐origin across a rainfall gradient.Crossref | GoogleScholarGoogle Scholar |

Losso A, Bär A, Dämon B, Dullin C, Ganthaler A, Petruzzellis F, Savi T, Tromba G, Nardini A, Mayr S (2018) Insights from in vivo micro‐CT analysis: testing the hydraulic vulnerability segmentation in Acer pseudoplatanus and Fagus sylvatica seedlings. New Phytologist 221, 1831–1842.
Insights from in vivo micro‐CT analysis: testing the hydraulic vulnerability segmentation in Acer pseudoplatanus and Fagus sylvatica seedlings.Crossref | GoogleScholarGoogle Scholar | 30347122PubMed |

Martin‐StPaul N, Delzon S, Cochard H (2017) Plant resistance to drought depends on timely stomatal closure. Ecology Letters 20, 1437–1447.
Plant resistance to drought depends on timely stomatal closure.Crossref | GoogleScholarGoogle Scholar | 28922708PubMed |

Meron M, Grimes D, Phene C, Davis K (1987) Pressure chamber procedures for leaf water potential measurements of cotton. Irrigation Science 8, 215–222.
Pressure chamber procedures for leaf water potential measurements of cotton.Crossref | GoogleScholarGoogle Scholar |

Nardini A, Salleo S (2000) Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylem cavitation? Trees 15, 14–24.
Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylem cavitation?Crossref | GoogleScholarGoogle Scholar |

Pivovaroff AL, Sack L, Santiago LS (2014) Coordination of stem and leaf hydraulic conductance in southern California shrubs: a test of the hydraulic segmentation hypothesis. New Phytologist 203, 842–850.
Coordination of stem and leaf hydraulic conductance in southern California shrubs: a test of the hydraulic segmentation hypothesis.Crossref | GoogleScholarGoogle Scholar | 24860955PubMed |

Pivovaroff AL, Cook VM, Santiago LS (2018) Stomatal behavior and stem xylem traits are coordinated for woody plant species under exceptional drought conditions. Plant, Cell & Environment 41, 2617–2626.
Stomatal behavior and stem xylem traits are coordinated for woody plant species under exceptional drought conditions.Crossref | GoogleScholarGoogle Scholar |

Rodriguez‐Dominguez CM, Carins Murphy MR, Lucani C, Brodribb TJ (2018) Mapping xylem failure in disparate organs of whole plants reveals extreme resistance in olive roots. New Phytologist 218, 1025–1035.
Mapping xylem failure in disparate organs of whole plants reveals extreme resistance in olive roots.Crossref | GoogleScholarGoogle Scholar | 29528498PubMed |

Santiago LS, Goldstein G, Meinzer FC, Fisher JB, Machado K, Woodruff D, Jones T (2004) Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia 140, 543–550.
Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees.Crossref | GoogleScholarGoogle Scholar | 15232729PubMed |

Schippers JH, Schmidt R, Wagstaff C, Jing HC (2015) Living to die and dying to live: the survival strategy behind leaf senescence. Plant Physiology 169, 914–930.
Living to die and dying to live: the survival strategy behind leaf senescence.Crossref | GoogleScholarGoogle Scholar | 26276844PubMed |

Scoffoni C, Albuquerque C, Brodersen C, Townes SV, John GP, Bartlett MK, Buckley TN, McElrone AJ, Sack L (2017) Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration. Plant Physiology 173, 1197–1210.
Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration.Crossref | GoogleScholarGoogle Scholar | 28049739PubMed |

Skelton RP, West AG, Dawson TE (2015) Predicting plant vulnerability to drought in biodiverse regions using functional traits. Proceedings of the National Academy of Sciences of the United States of America 112, 5744–5749.
Predicting plant vulnerability to drought in biodiverse regions using functional traits.Crossref | GoogleScholarGoogle Scholar | 25902534PubMed |

Skelton RP, Brodribb TJ, Choat B (2017) Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation. New Phytologist 214, 561–569.
Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation.Crossref | GoogleScholarGoogle Scholar | 28124474PubMed |

Sperry JS, Stiller V, Hacke UG (2003) Xylem hydraulics and the soil-plant-atmosphere continuum. Agronomy Journal 95, 1362–1370.
Xylem hydraulics and the soil-plant-atmosphere continuum.Crossref | GoogleScholarGoogle Scholar |

Sperry JS, Venturas MD, Anderegg WR, Mencuccini M, Mackay DS, Wang Y, Love DM (2017) Predicting stomatal responses to the environment from the optimization of photosynthetic gain and hydraulic cost. Plant, Cell & Environment 40, 816–830.
Predicting stomatal responses to the environment from the optimization of photosynthetic gain and hydraulic cost.Crossref | GoogleScholarGoogle Scholar |

Torres-Ruiz JM, Diaz-Espejo A, Perez-Martin A, Hernandez-Santana V (2015) Role of hydraulic and chemical signals in leaves, stems and roots in the stomatal behaviour of olive trees under water stress and recovery conditions. Tree Physiology 35, 415–424.
Role of hydraulic and chemical signals in leaves, stems and roots in the stomatal behaviour of olive trees under water stress and recovery conditions.Crossref | GoogleScholarGoogle Scholar | 25030936PubMed |

Tyree MT, Zimmermann MH (2002) ‘Xylem structure and the ascent of sap.’ (Springer: Berlin)

Tyree M, Cochard H, Cruiziat P, Sinclair B, Ameglio T (1993) Drought‐induced leaf shedding in walnut: evidence for vulnerability segmentation. Plant, Cell & Environment 16, 879–882.
Drought‐induced leaf shedding in walnut: evidence for vulnerability segmentation.Crossref | GoogleScholarGoogle Scholar |

Ullah A, Sun H, Yang X, Zhang X (2017) Drought coping strategies in cotton: increased crop per drop. Plant Biotechnology Journal 15, 271–284.
Drought coping strategies in cotton: increased crop per drop.Crossref | GoogleScholarGoogle Scholar | 28055133PubMed |

Urli M, Porté AJ, Cochard H, Guengant Y, Burlett R, Delzon S (2013) Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiology 33, 672–683.
Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees.Crossref | GoogleScholarGoogle Scholar | 23658197PubMed |

Venturas MD, Sperry JS, Hacke UG (2017) Plant xylem hydraulics: what we understand, current research, and future challenges. Journal of Integrative Plant Biology 59, 356–389.
Plant xylem hydraulics: what we understand, current research, and future challenges.Crossref | GoogleScholarGoogle Scholar | 28296168PubMed |

Wason JW, Anstreicher KS, Stephansky N, Huggett BA, Brodersen CR (2018) Hydraulic safety margins and air‐seeding thresholds in roots, trunks, branches and petioles of four northern hardwood trees. New Phytologist 219, 77–88.
Hydraulic safety margins and air‐seeding thresholds in roots, trunks, branches and petioles of four northern hardwood trees.Crossref | GoogleScholarGoogle Scholar | 29663388PubMed |

Willson CJ, Manos PS, Jackson RB (2008) Hydraulic traits are influenced by phylogenetic history in the drought‐resistant, invasive genus Juniperus (Cupressaceae). American Journal of Botany 95, 299–314.
Hydraulic traits are influenced by phylogenetic history in the drought‐resistant, invasive genus Juniperus (Cupressaceae).Crossref | GoogleScholarGoogle Scholar | 21632355PubMed |

Wolfe BT, Sperry JS, Kursar TA (2016) Does leaf shedding protect stems from cavitation during seasonal droughts? A test of the hydraulic fuse hypothesis. New Phytologist 212, 1007–1018.
Does leaf shedding protect stems from cavitation during seasonal droughts? A test of the hydraulic fuse hypothesis.Crossref | GoogleScholarGoogle Scholar | 27373446PubMed |

Yang S, Tyree MT (1994) Hydraulic architecture of Acer saccharum and A. rubrum: comparison of branches to whole trees and the contribution of leaves to hydraulic resistance. Journal of Experimental Botany 45, 179–186.
Hydraulic architecture of Acer saccharum and A. rubrum: comparison of branches to whole trees and the contribution of leaves to hydraulic resistance.Crossref | GoogleScholarGoogle Scholar |

Yi XP, Zhang YL, Yao HS, Luo HH, Gou L, Chow WS, Zhang WF (2016a) Different strategies of acclimation of photosynthesis, electron transport and antioxidative activity in leaves of two cotton species to water deficit. Functional Plant Biology 43, 448–460.
Different strategies of acclimation of photosynthesis, electron transport and antioxidative activity in leaves of two cotton species to water deficit.Crossref | GoogleScholarGoogle Scholar |

Yi XP, Zhang YL, Yao HS, Luo HH, Gou L, Chow WS, Zhang WF (2016b) Rapid recovery of photosynthetic rate following soil water deficit and re-watering in cotton plants (Gossypium herbaceum L.) is related to the stability of the photosystems. Journal of Plant Physiology 194, 23–34.
Rapid recovery of photosynthetic rate following soil water deficit and re-watering in cotton plants (Gossypium herbaceum L.) is related to the stability of the photosystems.Crossref | GoogleScholarGoogle Scholar | 26948982PubMed |

Zhang FP, Sussmilch F, Nichols DS, Cardoso AA, Brodribb TJ, McAdam SA (2018) Leaves, not roots or floral tissue, are the main site of rapid, external pressure-induced ABA biosynthesis in angiosperms. Journal of Experimental Botany 69, 1261–1267.
Leaves, not roots or floral tissue, are the main site of rapid, external pressure-induced ABA biosynthesis in angiosperms.Crossref | GoogleScholarGoogle Scholar | 29340606PubMed |

Zufferey V, Cochard H, Ameglio T, Spring JL, Viret O (2011) Diurnal cycles of embolism formation and repair in petioles of grapevine (Vitis vinifera cv. Chasselas). Journal of Experimental Botany 62, 3885–3894.
Diurnal cycles of embolism formation and repair in petioles of grapevine (Vitis vinifera cv. Chasselas).Crossref | GoogleScholarGoogle Scholar | 21447755PubMed |