Root architecture plasticity in response to drought stress in cotton revealed by a high-throughput automatic root phenotyping platform (HT-ARPP)

doi:10.1016/j.jia.2025.09.022

Advanced Online Publication | Current Issue | Archive | Adv Search

Simin Sun¹, Baoqi Li^1,²^#, Jiawei Shi¹, Linjie Xia¹, Haokun Wang¹, Yuxin Wang¹, Mengsi Gao¹, Junhao Wei¹, Wanneng Yang¹^#, Xianlong Zhang¹, Xiyan Yang¹^#

¹National Key Laboratory of Crop Genetic Improvement/National Center of Plant Gene Research (Wuhan)/Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, China

²State Key Lab for Conservation and Utilization of Subtropical Agri-Biological Resources/College of Agriculture, Guangxi University, Nanning 530004, China

Highlights

• High-throughput automatic root phenotyping of 228 upland cotton accessions under drought identified 27 image-based digital underground root traits (i-R_traits).

• A comprehensive drought-adaptability index (CIDA) classified root architectures into five groups and defined an ideal drought-adaptability root architecture.

• Medium/intermediate drought resistant cotton accessions are recommended as ideal breeding materials for cotton drought-resistance breeding.

Abstract
References

Download: PDF in ScienceDirect
Export: BibTeX | EndNote (RIS)

摘要

全球气候的剧烈变化引发了日益严峻的干旱胁迫，为农业生产和作物育种带来了巨大的挑战。根系作为感知胁迫信号的主要器官，在植物对土壤环境的干旱适应性方面发挥着至关重要的作用。因此，明确干旱条件下的最佳根系构型已成为作物育种的关键。本研究利用高通量自动化根系表型平台，将228份具有代表性的陆地棉自然群体材料在特定的根箱中培养，在苗期进行干旱胁迫处理，为期20天，进行了11次表型采集监测，通过自动化根系表型机器人采集了2万多张根系表型图，获得了27个基于图像的数字化根系性状指标。利用抗旱系数（DRC，即各个根系指标在干旱处理与对照处理下的比值）来评估不同指标对干旱胁迫的响应。结合根系性状分析计算其综合响应干旱胁迫指数（CIDA），并通过逐步回归分析建立了关键的根系性状模型，从而根据根系对干旱胁迫的适应性将自然群体材料分为5个类型。同时，通过地上部和地下部表型的综合分析，提出了棉花响应干旱胁迫的理想根系构型。研究结果表明，中度和中高度抗旱类型的棉花材料是在多变环境条件下保持稳定生长的理想育种材料，为未来以优化根系构型为目标的育种思路提供了新策略。

Abstract

Global climate change has intensified drought stress, presenting a significant challenge to agricultural production and breeding. The root system, as the primary organ sensing stress signals, plays a crucial role in determining plants' drought adaptability in soil conditions. Consequently, identifying optimal root architecture under drought conditions has become essential in crop breeding. This study employed a HT-ARPP to systematically analyze a natural population of 228 representative upland cotton accessions in specialized root boxes during seedling-stage drought stress. Root phenotypes were monitored 11 times across 20 days, generating over 20,000 images through an automatic root phenotypic robot, which yielded 27 image-based digital underground root traits (i-R_traits). The drought-resistant coefficient (DRC, ratio between drought and control of i-R_traits) was utilized to evaluate phenotypic responses. A comprehensive index of drought adaptability (CIDA) was developed through root traits analysis, and stepwise regression analysis established a model of key i-R_traits, enabling classification of accessions into 5 groups based on root adaptability to water deficiency. An ideal drought-adaptability root architecture was proposed through combined analysis of aboveground and underground phenotypes. The findings indicate that medium and intermediate drought resistant cotton accessions represent optimal breeding materials for maintaining stable growth under variable conditions, offering a novel strategy for future breeding programs focused on optimized root architecture.

Keywords: cotton drought resistance ideal drought-adaptability root architecture HT-ARPP

Online: 22 September 2025

Fund:

This work was supported by funding from the Development Fund for Xinjiang Talents XL (XL202402), China and the Agricultural Key Core Technology Research Project of Xinjiang Production and Construction Corps, China (NK2023AA102), and National Major Project on Agricultural Biological Breeding (2023ZD04039-01).

About author: #Correspondence Xiyan Yang, E-mail: yxy@mail.hzau.edu.cn; Baoqi Li, E-mail: bqli@gxu.edu.cn; Wanneng Yang, E-mail: ywn@mail.hzau.edu.cn

	Service
	E-mail this article
	Add to citation manager
	E-mail Alert
	RSS
	Articles by authors

Cite this article:

Simin Sun, Baoqi Li, Jiawei Shi, Linjie Xia, Haokun Wang, Yuxin Wang, Mengsi Gao, Junhao Wei, Wanneng Yang, Xianlong Zhang, Xiyan Yang. 2025. Root architecture plasticity in response to drought stress in cotton revealed by a high-throughput automatic root phenotyping platform (HT-ARPP). Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.09.022

Al-Tamimi N, Brien C, Oakey H, Berger B, Saade S, Ho Y S, Schmöckel S M, Tester M, Negrão S. 2016. Salinity tolerance loci revealed in rice using high-throughput non-invasive phenotyping. Nature Communications, 7, 13342.

Araus J L, Cairns J E. 2014. Field high-throughput phenotyping: The new crop breeding frontier. Trends in Plant Science, 19, 52-61.

Arvidsson S, Pérez-Rodríguez P, Mueller-Roeber B. 2011. A growth phenotyping pipeline for Arabidopsis thaliana integrating image analysis and rosette area modeling for robust quantification of genotype effects. New Phytologist, 191, 895-907.

Atkinson J A, Pound M P, Bennett M J, Wells D M. 2019. Uncovering the hidden half of plants using new advances in root phenotyping. Current Opinion in Biotechnology, 55, 1-8.

Atkinson J A, Wingen L U, Griffiths M, Pound M P, Gaju O, Foulkes M J, Le Gouis J, Griffiths S, Bennett M J, King J, Wells D M. 2015. Phenotyping pipeline reveals major seedling root growth QTL in hexaploid wheat. Journal of Experimental Botany, 66, 2283-2292.

Bellini C, Pacurar D I, Perrone I. 2014. Adventitious roots and lateral roots: Similarities and differences. Annual Review of Plant Biology, 65, 639-666.

Billah M, Li F, Yang Z. 2021. Regulatory network of cotton genes in response to salt, drought and wilt diseases (Verticillium and Fusarium): Progress and perspective. Frontiers in Plant Science, 12, 759245.

Cai G, Ahmed M A, Abdalla M, Carminati A. 2022. Root hydraulic phenotypes impacting water uptake in drying soils. Plant Cell and Environment, 45, 650-663.

Carley C N, Chen G, Das K K, Delory B M, Dimitrova A, Ding Y, George A P, Greeley L A, Han Q, Hendriks P W, Hernandez-Soriano M C, Li M, Ng J L P, Mau L, Mesa-Marín J, Miller A J, Rae A E, Schmidt J, Thies A, Topp C N, et al. 2022. Root biology never sleeps. New Phytologist, 235, 2149-2154.

Chen Q, Hu T, Li X, Song C, Zhu J, Chen L, Zhao Y. 2021. Phosphorylation of SWEET sucrose transporters regulates plant root: Shoot ratio under drought. Nature Plants, 8, 68-77.

Chen X, Liu P, Zhao B, Zhang J, Ren B, Li Z, Wang Z. 2022. Root physiological adaptations that enhance the grain yield and nutrient use efficiency of maize (Zea mays L) and their dependency on phosphorus placement depth. Field Crops Research, 276, 108378.

Colmer J, O'Neill C M, Wells R, Bostrom A, Reynolds D, Websdale D, Shiralagi G, Lu W, Lou Q, Le Cornu T, Ball J, Renema J, Flores Andaluz G, Benjamins R, Penfield S, Zhou J. 2020. SeedGerm: A cost-effective phenotyping platform for automated seed imaging and machine-learning based phenotypic analysis of crop seed germination. New Phytologist, 228, 778-793.

Correa J, Postma J A, Watt M, Wojciechowski T. 2019. Soil compaction and the architectural plasticity of root systems. Journal of Experimental Botany, 70, 6019-6034.

Daly K R, Tracy S R, Crout N M J, Mairhofer S, Pridmore T P, Mooney S J, Roose T. 2017. Quantification of root water uptake in soil using X-ray computed tomography and image-based modelling. Plant Cell and Environment, 41, 121-133.

Dietz K, Zörb C, Geilfus C. 2021. Drought and crop yield. Plant Biology, 23, 881-893.

Dinneny J R. 2019. Developmental responses to water and salinity in root systems. Annual Review of Cell and Developmental Biology, 35, 239-257.

Farooq M A, Gao S, Hassan M A, Huang Z, Rasheed A, Hearne S, Prasanna B, Li X, Li H. 2024. Artificial intelligence in plant breeding. Trends in Genetics, 40, 891-908.

Fry E L, Evans A L, Sturrock C J, Bullock J M, Bardgett R D. 2018. Root architecture governs plasticity in response to drought. Plant and Soil, 433, 189-200.

Gao J, Zhao Y, Zhao Z, Liu W, Jiang C, Li J, Zhang Z, Zhang H, Zhang Y, Wang X, Sun X, Li Z. 2023. RRS1 shapes robust root system to enhance drought resistance in rice. New Phytologist, 238, 1146-1162.

Ghosal S, Zheng B, Chapman S C, Potgieter A B, Jordan D R, Wang X, Singh A K, Singh A, Hirafuji M, Ninomiya S, Ganapathysubramanian B, Sarkar S, Guo W. 2019. A weakly supervised deep learning framework for sorghum head detection and counting. Plant Phenomics, 2019, 1525874.

Gioia T, Galinski A, Lenz H, Müller C, Lentz J, Heinz K, Briese C, Putz A, Fiorani F, Watt M, Schurr U, Nagel K A. 2017. GrowScreen-PaGe, a non-invasive, high-throughput phenotyping system based on germination paper to quantify crop phenotypic diversity and plasticity of root traits under varying nutrient supply. Functional Plant Biology, 44, 76-93.

Granier C, Aguirrezabal L, Chenu K, Cookson S J, Dauzat M, Hamard P, Thioux J J, Rolland G, Bouchier-Combaud S, Lebaudy A, Muller B, Simonneau T, Tardieu F. 2005. PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. New Phytologist, 169, 623-635.

Guo Z, Yang W, Chang Y, Ma X, Tu H, Xiong F, Jiang N, Feng H, Huang C, Yang P, Zhao H, Chen G, Liu H, Luo L, Hu H, Liu Q, Xiong L. 2018. Genome-wide association studies of image traits reveal genetic architecture of drought resistance in rice. Molecular Plant, 11, 789-805.

Guo C C, Sun H C, Bao X Y, Zhu L X, Zhang Y J, Zhang K, Li A C, Bai Z Y, Liu L T, Li C D. 2024.Increasing root-lower characteristics improves drought tolerance in cotton cultivars at the seedling stage. Journal of Integrative Agriculture, 23, 2242-2254.

Karlova R, Boer D, Hayes S, Testerink C. 2021. Root plasticity under abiotic stress. Plant Physiology, 187, 1057-1070.

Kochian L V. 2016. Root architecture. Journal of Integrative Plant Biology, 58, 190-192.

Konapala G, Mishra A K, Wada Y, Mann M E. 2020. Climate change will affect global water availability through compounding changes in seasonal precipitation and evaporation. Nature Communications, 11, 3044.

Li B, Chen L, Sun W, Wu D, Wang M, Yu Y, Chen G, Yang W, Lin Z, Zhang X, Duan L, Yang X. 2020. Phenomics‐based GWAS analysis reveals the genetic architecture for drought resistance in cotton. Plant Biotechnology Journal, 18, 2533-2544.

Liao Q, Chebotarov D, Islam M S, Quintana M R, Natividad M A, De Ocampo M, Beredo J C, Torres R O, Zhang Z, Song H, Price A H, McNally K L, Henry A. 2022. Aus rice root architecture variation contributing to grain yield under drought suggests a key role of nodal root diameter class. Plant Cell and Environment, 45, 854-870.

Liu Z, Qin T, Atienza M, Zhao Y, Nguyen H, Sheng H, Olukayode T, Song H, Panjvani K, Magalhaes J, Lucas W J, Kochian L V. 2023. Constitutive basis of root system architecture: Uncovering a promising trait for breeding nutrient- and drought-resilient crops. aBIOTECH, 4, 315-331.

Lynch J. 1995. Root architecture and plant productivity. Plant Physiology, 109, 7-13.

Lynch J P. 2007. Roots of the second green revolution. Australian Journal of Botany, 55, 493.

Lynch J P. 2013. Steep, cheap and deep: An ideotype to optimize water and N acquisition by maize root systems. Annals of Botany, 112, 347-357.

Maurel C, Nacry P. 2020. Root architecture and hydraulics converge for acclimation to changing water availability. Nature Plants, 6, 744-749.

Nadeem M, Li J, Yahya M, Sher A, Ma C, Wang X, Qiu L. 2019. Research progress and perspective on drought stress in legumes: A review. International Journal of Molecular Sciences, 20, 2541.

Nagel K A, Putz A, Gilmer F, Heinz K, Fischbach A, Pfeifer J, Faget M, Blossfeld S, Ernst M, Dimaki C, Kastenholz B, Kleinert A K, Galinski A, Scharr H, Fiorani F, Schurr U. 2012. GROWSCREEN-Rhizo is a novel phenotyping robot enabling simultaneous measurements of root and shoot growth for plants grown in soil-filled rhizotrons. Functional Plant Biology, 39, 891.

De Nittis M, De Vivo M, Dello Ioio R, Sabatini S. 2025. Hormonal regulation of primary root development. Cell Reports, 44, 115751.

Osmont K S, Sibout R, Hardtke C S. 2007. Hidden branches: Developments in root system architecture. Annual Review of Plant Biology, 58, 93-113.

Potgieter A B, George-Jaeggli B, Chapman S C, Laws K, Suárez Cadavid L A, Wixted J, Watson J, Eldridge M, Jordan D R, Hammer G L. 2017. Multi-spectral imaging from an unmanned aerial vehicle enables the assessment of seasonal leaf area dynamics of sorghum breeding lines. Frontiers in Plant Science, 8, 1532.

Puig J, Pauluzzi G, Guiderdoni E, Gantet P. 2012. Regulation of shoot and root development through mutual signaling. Molecular Plant, 5, 974-983.

Rellán-Álvarez R, Lobet G, Lindner H, Pradier P L, Sebastian J, Yee M C, Geng Y, Trontin C, LaRue T, Schrager-Lavelle A, Haney C H, Nieu R, Maloof J, Vogel J P, Dinneny J R. 2015. GLO-Roots: An imaging platform enabling multidimensional characterization of soil-grown root systems. Elife, 4, e07597.

Sallam A, Alqudah A M, Dawood M F A, Baenziger P S, Börner A. 2019. Drought stress tolerance in wheat and barley: Advances in physiology, breeding and genetics research. International Journal of Molecular Sciences, 20, 3137.

Sarić R, Nguyen V D, Burge T, Berkowitz O, Trtílek M, Whelan J, Lewsey M G, Čustović E. 2022. Applications of hyperspectral imaging in plant phenotyping. Trends in Plant Science, 27, 301-315.

Schachtman D P, Goodger J Q. 2008. Chemical root to shoot signaling under drought. Trends in Plant Science, 13, 281-287.

Seethepalli A, Guo H, Liu X, Griffiths M, Almtarfi H, Li Z, Liu S, Zare A, Fritschi F B, Blancaflor E B, Ma X F, York L M. 2020. RhizoVision crown: An integrated hardware and software platform for root crown phenotyping. Plant Phenomics, 2020, 3074916.

Sheoran S, Kaur Y, Kumar S, Shukla S, Rakshit S, Kumar R. 2022. Recent advances for drought stress tolerance in maize (Zea mays L.): Present status and future prospects. Frontiers in Plant Science, 13, 872566.

Shoaib M, Banerjee B P, Hayden M, Kant S. 2022. Roots’ drought adaptive traits in crop improvement. Plants, 11, 2256.

Singh A K, Ganapathysubramanian B, Sarkar S, Singh A. 2018. Deep learning for plant stress phenotyping: Trends and future perspectives. Trends in Plant Science, 23, 883-898.

Smith S, De Smet I. 2012. Root system architecture: Insights from Arabidopsis and cereal crops. Philosophical Transactions of the Royal Society B (Biological Sciences), 367, 1441-1452.

Sun S M, Han B, Chen L, Sun W N, Zhang X L, Yang X Y. 2022. Root system architecture analysis and genome-wide association study of root system architecture related traits in cotton. Acta Agronomica Sinica, 48, 1081-1090. (in Chinese)

Szira F, Bálint A, Börner A. 2008. Evaluation of drought-related traits and screening methods at different developmental stages in spring barley. Journal of Agronomy and Crop Science, 194, 334-342.

Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J, Matsumoto T, Takai T, Okuno K, Yano M. 2013. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genetics, 45, 1097-1102.

Ullah A, Sun H, Yang X, Zhang X. 2017. Drought coping strategies in cotton: Increased crop per drop. Plant Biotechnology Journal, 15, 271-284.

Wasson A P, Richards R A, Chatrath R, Misra S C, Prasad S V S, Rebetzke G J, Kirkegaard J A, Christopher J, Watt M. 2012. Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. Journal of Experimental Botany, 63, 3485-3498.

Wen X, Chen Z, Yang Z, Wang M, Jin S, Wang G, Zhang L, Wang L, Li J, Saeed S, He S, Wang Z, Wang K, Kong Z, Li F, Zhang X, Chen X, Zhu Y. 2023. A comprehensive overview of cotton genomics, biotechnology and molecular biological studies. Science China (Life Sciences), 66, 2214-2256.

Williams A, de Vries F T. 2019. Plant root exudation under drought: Implications for ecosystem functioning. New Phytologist, 225, 1899-1905.

Wu D, Guo Z, Ye J, Feng H, Liu J, Chen G, Zheng J, Yan D, Yang X, Xiong X, Liu Q, Niu Z, Gay A P, Doonan J H, Xiong L, Yang W. 2018. Combining high-throughput micro-CT-RGB phenotyping and genome-wide association study to dissect the genetic architecture of tiller growth in rice. Journal of Experimental Botany, 70, 545-561.

Wu J, Wu Q, Pagès L, Yuan Y, Zhang X, Du M, Tian X, Li Z. 2018. RhizoChamber-Monitor: A robotic platform and software enabling characterization of root growth. Plant Methods, 14, 44.

Wu X, Feng H, Wu D, Yan S, Zhang P, Wang W, Zhang J, Ye J, Dai G, Fan Y, Li W, Song B, Geng Z, Yang W, Chen G, Qin F, Terzaghi W, Stitzer M, Li L, Xiong L, et al. 2021. Using high-throughput multiple optical phenotyping to decipher the genetic architecture of maize drought tolerance. Genome Biology, 22, 185.

Xiong R, Liu S, Considine M J, Siddique K H M, Lam H M, Chen Y. 2020. Root system architecture, physiological and transcriptional traits of soybean (Glycine max L.) in response to water deficit: A review. Plant Physiology, 172, 405-418.

Yang W, Guo Z, Huang C, Duan L, Chen G, Jiang N, Fang W, Feng H, Xie W, Lian X, Wang G, Luo Q, Zhang Q, Liu Q, Xiong L. 2014. Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice. Nature Communications, 5, 5087.

Yang Z, Qin F. 2023. The battle of crops against drought: Genetic dissection and improvement. Journal of Integrative Plant Biology, 65, 496-525.

York L M, Nord E A, Lynch J P. 2013. Integration of root phenes for soil resource acquisition. Frontiers in Plant Science, 4, 355.

Zhang Y J, Wu X, Wang X R, Dai M Q, Peng Y L. 2025. Crop root system architecture in drought response. Journal of Genetics and Genomics, 52, 4-13.

Zhang Y Y, Zhao Y J, Hou X Y, Zhang C L, Wang Z Y, Zhang J Q, Liu X C, Shi X C, Duan W R, Xiao K. 2025. Wheat TaPYL9-involved signalling pathway impacts plant drought response through regulating distinct osmotic stress-associated physiological indices. Plant Biotechnology Journal, 23, 352-373.

Zheng C, Bochmann H, Liu Z, Kant J, Schrey S D, Wojciechowski T, Postma J A. 2023. Plant root plasticity during drought and recovery: What do we know and where to go? Frontiers in Plant Science, 14, 1084355.

Zhu J K. 2016. Abiotic stress signaling and responses in plants. Cell, 167, 313-324.

No related articles found!

No Suggested Reading articles found!

Viewed

Full text

Abstract

Cited

Shared

Discussed

Cite this article:

About JIA

Editorial board

For authors