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

Morpho-physiological adaptations to weed competition impair green bean (Phaseolus vulgaris) ability to overcome moderate salt stress

Valerio Cirillo https://orcid.org/0000-0002-2929-5485 A * , Marco Esposito B , Matteo Lentini A , Claudio Russo A , Nausicaa Pollaro A and Albino Maggio A
+ Author Affiliations
- Author Affiliations

A Department of Agricultural Sciences, University of Naples Federico II, Via Università 100, Portici 80055, Italy.

B Group of Agroecology, Institute of Life Sciences, Scuola Superiore Sant’Anna, Pisa, Italy.

* Correspondence to: valerio.cirillo@unina.it

Handling Editor: Jairo Palta

Functional Plant Biology 51, FP23202 https://doi.org/10.1071/FP23202
Submitted: 5 September 2023  Accepted: 1 May 2024  Published: 20 May 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

The two stresses of weed competition and salt salinity lead to crop yield losses and decline in the productivity of agricultural land. These constraints threaten the future of food production because weeds are more salt stress tolerant than most crops. Climate change will lead to an increase of soil salinity worldwide, and possibly exacerbate the competition between weeds and crops. This aspect has been scarcely investigated in the context of weed-crop competition. Therefore, we conducted a field experiment on green beans (Phaseolus vulgaris) to investigate the combined impact of weed competition and salt stress on key morpho-physiological traits, and crop yield. We demonstrated that soil salinity shifted weed composition toward salt tolerant weed species (Portulaca oleracea and Cynodon dactylon), while it reduced the presence of lower tolerance species. Weed competition activated adaptation responses in green bean such as reduced leaf mass per area and biomass allocation to the stem, unchanged stomatal density and instantaneous water use efficiency, which diverge from those that are typically observed as a consequence of salt stress. The morpho-physiological modifications caused by weeds is attributed to the alterations of light intensity and/or quality, further confirming the pivotal role of the light in crop response to weeds. We concluded that higher yield loss caused by combined salt stress and weed competition is due to impaired morpho-physiological responses, which highlights the negative interaction between salt stress and weed competition. This phenomenon will likely be more frequent in the future, and potentially reduce the efficacy of current weed control methods.

Keywords: abiotic stress, biotic stress, combined stress, open field, stress response, stress tolerance, weed-crop competition, weed dynamics.

References

Ábrahám E, Rigó G, Székely G, Nagy R, Koncz C, Szabados L (2003) Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis. Plant Molecular Biology 51, 363-372.
| Crossref | Google Scholar | PubMed |

Ali A, Raddatz N, Aman R, Kim S, Park HC, Jan M, Baek D, Khan IU, Oh D-H, Lee SY, Bressan RA, Lee KW, Maggio A, Pardo JM, Bohnert HJ, Yun D-J (2016) A single amino-acid substitution in the sodium transporter HKT1 associated with plant salt tolerance. Plant Physiology 171, 2112-2126.
| Crossref | Google Scholar | PubMed |

Allen RG, Pereira LS, Raes D, Smith M (1998) Crop evapotranspiration: guidelines for computing crop water requirements. Irrigation and Drainage Paper. No. 56. p. 300. FAO, Rome, Italy.

Almeida DM, Oliveira MM, Saibo NJM (2017) Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants. Genetics and Molecular Biology 40, 326-345.
| Crossref | Google Scholar | PubMed |

Amores MJ, Verones F, Raptis C, Juraske R, Pfister S, Stoessel F, Antón A, Castells F, Hellweg S (2013) Biodiversity impacts from salinity increase in a coastal wetland. Environmental Science & Technology 47, 6384-6392.
| Crossref | Google Scholar | PubMed |

Asgarpour R, Ghorbani R, Khajeh-Hosseini M, Mohammadvand E, Chauhan BS (2015) Germination of spotted spurge (Chamaesyce maculata) seeds in response to different environmental factors. Weed Science 63, 502-510.
| Crossref | Google Scholar |

Ballaré CL, Pierik R (2017) The shade-avoidance syndrome: multiple signals and ecological consequences. Plant, Cell & Environment 40, 2530-2543.
| Crossref | Google Scholar |

Barbieri G, Vallone S, Orsini F, Paradiso R, De Pascale S, Negre-Zakharov F, Maggio A (2012) Stomatal density and metabolic determinants mediate salt stress adaptation and water use efficiency in basil (Ocimum basilicum L.). Journal of Plant Physiology 169, 1737-1746.
| Crossref | Google Scholar | PubMed |

Bilalis D, Karkanis A, Savvas D, Kontopoulou C-K, Efthimiadou A (2014) Effects of fertilization and salinity on weed flora in common bean (Phaseolus vulgaris L.) grown following organic or conventional cultural practices. Australian Journal of Crop Science 8, 178-182.
| Google Scholar |

Bocchini M, Bartucca ML, Ciancaleoni S, Mimmo T, Cesco S, Pii Y, Albertini E, Del Buono D (2015) Iron deficiency in barley plants: phytosiderophore release, iron translocation, and DNA methylation. Frontiers in Plant Science 6, 514.
| Crossref | Google Scholar | PubMed |

Bouraoui D, Cekstere G, Osvalde A, Vollenweider P, Rasmann S (2019) Deicing salt pollution affects the foliar traits and arthropods’ biodiversity of lime trees in Riga’s street greeneries. Frontiers in Ecology and Evolution 7, 282.
| Crossref | Google Scholar |

Briggs SV, Taws N (2003) Impacts of salinity on biodiversity – clear understanding or muddy confusion? Australian Journal of Botany 51, 609-617.
| Crossref | Google Scholar |

Cai Z-Q, Gao Q (2020) Comparative physiological and biochemical mechanisms of salt tolerance in five contrasting highland quinoa cultivars. BMC Plant Biology 20, 70.
| Crossref | Google Scholar |

Cheeseman JM (2015) The evolution of halophytes, glycophytes and crops, and its implications for food security under saline conditions. New Phytologist 206, 557-570.
| Crossref | Google Scholar | PubMed |

Cirillo V, Masin R, Maggio A, Zanin G (2018) Crop-weed interactions in saline environments. European Journal of Agronomy 99, 51-61.
| Crossref | Google Scholar |

Cirillo V, D’Amelia V, Esposito M, Amitrano C, Carillo P, Carputo D, Maggio A (2021) anthocyanins are key regulators of drought stress tolerance in tobacco. Biology 10, 139.
| Crossref | Google Scholar | PubMed |

Clements DR, DiTommaso A (2011) Climate change and weed adaptation: can evolution of invasive plants lead to greater range expansion than forecasted? Weed Research 51, 227-240.
| Crossref | Google Scholar |

Corwin DL (2021) Climate change impacts on soil salinity in agricultural areas. European Journal of Soil Science 72, 842-862.
| Crossref | Google Scholar |

Courbier S, Pierik R (2019) Canopy light quality modulates stress responses in plants. IScience 22, 441-452.
| Crossref | Google Scholar | PubMed |

De Pascale S, Orsini F, Caputo R, Palermo MA, Barbieri G, Maggio A (2012) Seasonal and multiannual effects of salinisation on tomato yield and fruit quality. Functional Plant Biology 39, 689-698.
| Crossref | Google Scholar | PubMed |

Di Stasio E, Cirillo V, Raimondi G, Giordano M, Esposito M, Maggio A (2020) Osmo-priming with seaweed extracts enhances yield of salt-stressed tomato plants. Agronomy 10, 1559.
| Crossref | Google Scholar |

Du L, Gao X, Qu C, Bai S, Shi C, Jiang X, Li X, Ju Q, Qu M (2022) Identification of purple nutsedge (Cyperus rotundus L.) ecotypes and the effect of environmental factors on tuber sprouting in China. Weed Research 62, 360-371.
| Crossref | Google Scholar |

El-Nakhel C, Pannico A, Kyriacou MC, Petropoulos SA, Giordano M, Colla G, Troise AD, Vitaglione P, De Pascale S, Rouphael Y (2020) Dataset on the organic acids, sulphate, total nitrogen and total chlorophyll contents of two lettuce cultivars grown hydroponically using nutrient solutions of variable macrocation ratios. Data in Brief 29, 105135.
| Crossref | Google Scholar | PubMed |

EL Sabagh A, Islam MS, Skalicky M, Ali Raza M, Singh K, Anwar Hossain M, Hossain A, Mahboob W, Iqbal MA, Ratnasekera D, Singhal RK, Ahmed S, Kumari A, Wasaya A, Sytar O, Brestic M, ÇIG F, Erman M, Habib Ur Rahman M, Ullah N, Arshad A (2021) Salinity stress in wheat (Triticum aestivum L.) in the changing climate: adaptation and management strategies. Frontiers in Agronomy 3, 661932.
| Crossref | Google Scholar |

Feng L, Chen G-Q, Tian X-S, Yang H-M, Yue M-F, Yang C-H (2015) The hotter the weather, the greater the infestation of Portulaca oleracea: opportunistic life-history traits in a serious weed. Weed Research 55, 396-405.
| Crossref | Google Scholar |

Feng XJ, Li JR, Qi SL, Lin QF, Jin JB, Hua XJ (2016) Light affects salt stress-induced transcriptional memory of P5CS1 in Arabidopsis. Proceedings of the National Academy of Sciences 113, E8335-E8343.
| Crossref | Google Scholar |

Fernandez ON (2003) Establishment of Cynodon dactylon from stolon and rhizome fragments. Weed Research 43, 130-138.
| Crossref | Google Scholar |

Fernández-Milmanda GL, Ballaré CL (2021) Shade avoidance: expanding the color and hormone palette. Trends in Plant Science 26, 509-523.
| Crossref | Google Scholar | PubMed |

Fogliatto S, Ferrero A, Vidotto F (2020) How can weedy rice stand against abiotic stresses? A review. Agronomy 10, 1284.
| Crossref | Google Scholar |

Ghirardelli A, Schiavon M, Zanin G, Ostapczuk P, Masin R (2021) Short-term responses to salinity of soybean and Chenopodium album grown in single and mixed-species hydroponic systems. Agronomy 11, 1481.
| Crossref | Google Scholar |

Giorio P, Cirillo V, Caramante M, Oliva M, Guida G, Venezia A, Grillo S, Maggio A, Albrizio R (2020) Physiological basis of salt stress tolerance in a landrace and a commercial variety of sweet pepper (Capsicum annuum L.). Plants 9, 795.
| Crossref | Google Scholar | PubMed |

Hadi MR, Karimi N (2012) The role of calcium in plants’ salt tolerance. Journal of Plant Nutrition 35, 2037-2054.
| Crossref | Google Scholar |

Haj-Amor Z, Araya T, Kim D-G, Bouri S, Lee J, Ghiloufi W, Yang Y, Kang H, Jhariya MK, Banerjee A, Lal R (2022) Soil salinity and its associated effects on soil microorganisms, greenhouse gas emissions, crop yield, biodiversity and desertification: a review. Science of The Total Environment 843, 156946.
| Crossref | Google Scholar |

Hayes S, Pantazopoulou CK, van Gelderen K, Reinen E, Tween AL, Sharma A, de Vries M, Prat S, Schuurink RC, Testerink C, Pierik R (2019) Soil salinity limits plant shade avoidance. Current Biology 29, 1669-1676.e4.
| Crossref | Google Scholar |

Horvath DP, Bruggeman S, Moriles-Miller J, Anderson JV, Dogramaci M, Scheffler BE, Hernandez AG, Foley ME, Clay S (2018) Weed presence altered biotic stress and light signaling in maize even when weeds were removed early in the critical weed-free period. Plant Direct 2, e00057.
| Crossref | Google Scholar |

Horvath DP, Clay SA, Swanton CJ, Anderson JV, Chao WS (2023) Weed-induced crop yield loss: a new paradigm and new challenges. Trends in Plant Science 28, 567-582.
| Crossref | Google Scholar | PubMed |

Hu YB, Sperotto RA (2021) Regulatory hubs in plant stress adaptation. Plant Biology 23, 3-6.
| Crossref | Google Scholar | PubMed |

Humphries T, Graz FF, Florentine SK (2018) Factors effecting the germination and emergence of a rangeland weed; European heliotrope (Heliotropium europaeum L.). The Rangeland Journal 40, 583-590.
| Crossref | Google Scholar |

Jaarsma R, de Vries RSM, de Boer AH (2013) Effect of salt stress on growth, Na+ accumulation and proline metabolism in potato (Solanum tuberosum) cultivars. PLoS ONE 8, e60183.
| Crossref | Google Scholar |

Jespersen E, Kirk GH, Brix H, Eller F, Sorrell BK (2021) Shade and salinity responses of two dominant coastal wetland grasses: implications for light competition at the transition zone. Annals of Botany 128, 469-480.
| Crossref | Google Scholar |

Karakas S, Bolat I, Dikilitas M (2021) The use of halophytic companion plant (Portulaca oleracea L.) on some growth, fruit, and biochemical parameters of strawberry plants under salt stress. Horticulturae 7, 63.
| Crossref | Google Scholar |

Karkanis A, Ntatsi G, Alemardan A, Petropoulos S, Bilalis D (2018) Interference of weeds in vegetable crop cultivation, in the changing climate of Southern Europe with emphasis on drought and elevated temperatures: a review. The Journal of Agricultural Science 156, 1175-1185.
| Crossref | Google Scholar |

Kaur S, Kaur R, Chauhan BS (2018) Understanding crop-weed-fertilizer-water interactions and their implications for weed management in agricultural systems. Crop Protection 103, 65-72.
| Crossref | Google Scholar |

Kiani-Pouya A, Rasouli F, Rabbi B, Falakboland Z, Yong M, Chen Z-H, Zhou M, Shabala S (2020) Stomatal traits as a determinant of superior salinity tolerance in wild barley. Journal of Plant Physiology 245, 153108.
| Crossref | Google Scholar | PubMed |

Kissoudis C, van de Wiel C, Visser RGF, van der Linden G (2014) Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk. Frontiers in Plant Science 5, 207.
| Crossref | Google Scholar |

Liao Q, Gu S, Kang S, Du T, Tong L, Wood JD, Ding R (2022) Mild water and salt stress improve water use efficiency by decreasing stomatal conductance via osmotic adjustment in field maize. Science of The Total Environment 805, 150364.
| Crossref | Google Scholar | PubMed |

Liu JG, Mahoney KJ, Sikkema PH, Swanton CJ (2009) The importance of light quality in crop-weed competition. Weed Research 49, 217-224.
| Crossref | Google Scholar |

Liu X, Mak M, Babla M, Wang F, Chen G, Veljanoski F, Wang G, Shabala S, Zhou M, Chen Z-H (2014) Linking stomatal traits and expression of slow anion channel genes HvSLAH1 and HvSLAC1 with grain yield for increasing salinity tolerance in barley. Frontiers in Plant Science 5, 634.
| Crossref | Google Scholar |

Liu H, Todd JL, Luo H (2023) Turfgrass salinity stress and tolerance – a review. Plants 12, 925.
| Crossref | Google Scholar | PubMed |

Lozano-Isla F, Campos MLO, Endres L, Bezerra-Neto E, Pompelli MF (2018) Effects of seed storage time and salt stress on the germination of Jatropha curcas L. Industrial Crops and Products 118, 214-224.
| Crossref | Google Scholar |

MacLaren C, Storkey J, Menegat A, Metcalfe H, Dehnen-Schmutz K (2020) An ecological future for weed science to sustain crop production and the environment. A review. Agronomy for Sustainable Development 40, 24.
| Crossref | Google Scholar |

Magallon KJ, Dinneny JR (2019) Environmental stress: salinity ruins a plant’s day in the sun. Current Biology 29, R360-R362.
| Crossref | Google Scholar | PubMed |

Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan ML, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play an active role in stress-induced growth reduction? The Plant Journal 31, 699-712.
| Crossref | Google Scholar |

Marsack JM, Connolly BM (2022) Generalist herbivore response to volatile chemical induction varies along a gradient in soil salinization. Scientific Reports 12, 1689.
| Crossref | Google Scholar |

Maxwell BD, Luschei E (2004) The ecology of crop-weed interactions. Journal of Crop Improvement 11, 137-151.
| Crossref | Google Scholar |

Mehra P, Pandey BK, Giri J (2017) Improvement in phosphate acquisition and utilization by a secretory purple acid phosphatase (OsPAP21b) in rice. Plant Biotechnology Journal 15, 1054-1067.
| Crossref | Google Scholar | PubMed |

Nevo E, Chen G (2010) Drought and salt tolerances in wild relatives for wheat and barley improvement. Plant, Cell & Environment 33, 670-685.
| Crossref | Google Scholar | PubMed |

Panchal P, Miller AJ, Giri J (2021) Organic acids: versatile stress-response roles in plants. Journal of Experimental Botany 72, 4038-4052.
| Crossref | Google Scholar | PubMed |

Pandey P, Ramegowda V, Senthil-Kumar M (2015) Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms. Frontiers in Plant Science 6, 723.
| Crossref | Google Scholar |

Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182, 565-588.
| Crossref | Google Scholar | PubMed |

Praxedes SC, De Lacerda CF, DaMatta FM, Prisco JT, Gomes-Filho E (2010) Salt tolerance is associated with differences in ion accumulation, biomass allocation and photosynthesis in cowpea cultivars. Journal of Agronomy and Crop Science 196, 193-204.
| Crossref | Google Scholar |

Rengel Z (2015) Availability of Mn, Zn and Fe in the rhizosphere. Journal of Soil Science and Plant Nutrition 15, 397-409.
| Google Scholar |

Ruggiero B, Koiwa H, Manabe Y, Quist TM, Inan G, Saccardo F, Joly RJ, Hasegawa PM, Bressan RA, Maggio A (2004) Uncoupling the effects of abscisic acid on plant growth and water relations. Analysis of sto1/nced3, an abscisic acid-deficient but salt stress-tolerant mutant in Arabidopsis. Plant Physiology 136, 3134-3147.
| Crossref | Google Scholar | PubMed |

Schambow TJ, Adjesiwor AT, Lorent L, Kniss AR (2019) Shade avoidance cues reduce Beta vulgaris growth. Weed Science 67, 311-317.
| Crossref | Google Scholar |

Shabala S, Hariadi Y, Jacobsen S-E (2013) Genotypic difference in salinity tolerance in quinoa is determined by differential control of xylem Na+ loading and stomatal density. Journal of Plant Physiology 170, 906-914.
| Crossref | Google Scholar | PubMed |

Shao A, Wang W, Fan S, Xu X, Yin Y, Erick A, Li X, Wang G, Wang H, Fu J (2021) Comprehensive transcriptional analysis reveals salt stress-regulated key pathways, hub genes and time-specific responsive gene categories in common bermudagrass (Cynodon dactylon (L.) Pers.) roots. BMC Plant Biology 21, 175.
| Crossref | Google Scholar |

Sharma G, Barney JN, Westwood JH, Haak DC (2021) Into the weeds: new insights in plant stress. Trends in Plant Science 26, 1050-1060.
| Crossref | Google Scholar | PubMed |

Suzuki A, Suriyagoda L, Shigeyama T, Tominaga A, Sasaki M, Hiratsuka Y, Yoshinaga A, Arima S, Agarie S, Sakai T, Inada S, Jikumaru Y, Kamiya Y, Uchiumi T, Abe M, Hashiguchi M, Akashi R, Sato S, Kaneko T, Tabata S, Hirsch AM (2011) Lotus japonicus nodulation is photomorphogenetically controlled by sensing the red/far red (R/FR) ratio through jasmonic acid (JA) signaling. Proceedings of the National Academy of Sciences of the United States of America 108, 16837-16842.
| Crossref | Google Scholar |

Tanveer M, Shah AN (2017) An insight into salt stress tolerance mechanisms of Chenopodium album. Environmental Science and Pollution Research 24, 16531-16535.
| Crossref | Google Scholar | PubMed |

Trognitz F, Hackl E, Widhalm S, Sessitsch A (2016) The role of plant–microbiome interactions in weed establishment and control. FEMS Microbiology Ecology 92, fiw138.
| Crossref | Google Scholar |

van Dijk M, Morley T, Rau ML, Saghai Y (2021) A meta-analysis of projected global food demand and population at risk of hunger for the period 2010–2050. Nature Food 2, 494-501.
| Crossref | Google Scholar | PubMed |

Wang Z, Hong Y, Zhu G, Li Y, Niu Q, Yao J, Hua K, Bai J, Zhu Y, Shi H, Huang S, Zhu J-K (2020) Loss of salt tolerance during tomato domestication conferred by variation in a Na+/K+ transporter. The EMBO Journal 39, e103256.
| Crossref | Google Scholar |

Xu T, Niu J, Jiang Z (2022) Sensing mechanisms: calcium signaling mediated abiotic stress in plants. Frontiers in Plant Science 13, 925863.
| Crossref | Google Scholar |

Yang X-Y, Zhang Z-W, Fu Y-F, Feng L-Y, Li M-X, Kang Q, Wang C-Q, Yuan M, Chen Y-E, Tao Q, Lan T, Tang X-Y, Chen G-D, Zeng J, Yuan S (2022a) Shade avoidance 3 mediates crosstalk between shade and nitrogen in arabidopsis leaf development. Frontiers in Plant Science 12, 800913.
| Crossref | Google Scholar |

Yang C, Tang W, Sun J, Guo H, Sun S, Miao F, Yang G, Zhao Y, Wang Z, Sun J (2022b) Weeds in the alfalfa field decrease rhizosphere microbial diversity and association networks in the North China Plain. Frontiers in Microbiology 13, 840774.
| Crossref | Google Scholar |