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Gene pyramiding improved cell membrane stability under heat stress in cotton (Gossypium hirsutum L.)

BMC Plant Biology volume 24, Article number: 886 (2024) Cite this article

Abstract

Climate change has been drastically affecting cotton not only in Pakistan but also all over the world. Normally cotton is known as heat tolerant when compared with other crops, but if the high temperature occurs during flowering period the yield decreases significantly. Marker assisted gene pyramiding provides a sustainable solution to improve heat tolerance. A total of seven genotypes were developed by a series of crossing seven tolerant genotypes over the period of three years. Tolerant genotypes were selected by screening for important transcription factors (GHSP26, HSP3, HSFA2, DREB1A, HSP101, DREB2A, GhNAC2, HSPCB, GhWRKY41, TPS, GbMYB5, ANNAT8, GhMPK17, GhMKK1, GhMKK3, GhMPK2, HSC70, APX1 and GhPP2A1). The seven genotypes were evaluated under normal and heat stress in a multi-year trial. The traits related to heat tolerance, such as cell membrane stability, relative water content, excised leaf water loss, plant height, number of nodes, internodal length, number of buds, number of bolls and leaf area was observed under normal and heat stress conditions. The developed genotypes showed improvement in cell membrane stability and relative water content under heat stress. The genotypes [(VH-305×MNH-886)×MNH-1035)×NIAB-78)], [(MNH-1035×MNH-886)×MNH-886)×SM-431] and [(MNH-1035×MNH-886)×MNH-886)×SS-32] depicted heat tolerance and could be used as heat tolerant material for variety development in breeding programs.

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Introduction

The average annual temperature of Pakistan has witnessed an increasing trend from 1997 onward with an average annual increase of more than 1 °C [1]. 1 °C increase in the temperature can lead to the decline of cotton production about 5519 tons in Pakistan [2]. The country may face 2.5 °C increase in temperature by 2050. Several researchers have suggested that Pakistan is anticipated to suffer world’s largest agricultural output losses as a result of present trends and predicted climate change scenarios [3]. Temperature changes seriously affect cotton phenology and production under climate change [4]. High temperature stress conditions cause water deficit in tissues, leading to relative cell injury, a decrease in transpiration, enzymes, and ion uptake and transport [5], a decrease in shoot dry mass, growth, and net assimilation rates [6], pre-and post-harvest damage, protein denaturation, cell death, enzyme inactivation. Heat stress is defined as a brief and sharp rise in soil and air temperature that harms plant growth and development permanently. The interaction of environmental conditions and abiotic stressors, such as drought, salt, waterlogging, and high heat, leads to a 50% reduction in cotton output and a considerable decline in lint quality [7]. High temperature stress is a major determinant in crop development and output. Heat waves, as well as a rise in the frequency of warm days and nights, have become increasingly common in most parts of the world. Cotton, being a semiarid crop, is extremely susceptible to high temperatures during the reproductive phases. The combination of high temperatures and cotton reproductive phases is a key impediment to achieving yield potential in the subcontinent. Since May-June temperatures of 47 °C and higher, along with high humidity in July-August, provide a particularly difficult environment for cotton, affecting all reproductive phases of the cotton crop.

The development of heat tolerant genotypes is a sustainable solution to avoid economic losses. Heat tolerance in cotton is a complex quantitative trait. Marker assisted gene pyramiding is one of the most reliable procedures aimed at assembling multiple desirable genes from multiple parents with known effects on target traits into a single genotype. The end product of a gene pyramiding program is a genotype with all of the target genes. It is mainly used in improving existing elite cultivars for a few unsatisfactory traits, for which genes with large positive effects are identified. Its first part is called a pedigree, which aims at cumulating of all target genes in a single genotype called the root genotype. The second part is called the fixation step, which aims at fixing the target genes into a homozygous state i.e., to derive the ideal genotype from the one single genotype.

Gene pyramiding has been in practice previously for major crops, including such as in wheat for stem resistance [8, 9], powdery mildew [10], stripe resistance [11], and leaf rust resistance [12]. In Rice, for bacterial blight [13], BLB and high amylose content [14], cold tolerance [15], blast resistance [16, 17]. In Cotton, bollworm resistance has been achieved through gene pyramiding [18].

Heat tolerance in cotton is a quantitative trait so it is difficult to transfer to a new genotype and is mostly conferred through heat shock protein (HSP) genes. The synthesis of heat shock protein-inducing factors in response to high temperatures results in the transcription of heat shock proteins. It appears that the HSPs are involved in the mechanisms protecting the membrane integrity of heat resistant genotypes. Heat stress may trigger the early initiation of HSP gene transcription, but in heat sensitive genotypes, expression declines as the duration of the stress lengthens [19]. The expression of some HSP genes may enhance heat tolerance by resulting in the creation of heat shock proteins [20]. The HSP100 and small HSPs play an important role in thermo tolerance, protein disaggregation, etc., whereas HSP90 and small HSPs help in the stabilization of miss folded protein and interact with other signaling molecules. The Hsp70 and HSP60 assist in the proper folding of proteins [21]. Breeders have studied the functional description of genes and the interacting pathways accountable for controlling drought tolerance in cotton. Hundreds of genes/QTL have been identified, and many have been cloned for drought tolerance in cotton [22].

Mostly gene pyramiding is done against biotic stresses and very little work is done regarding abiotic stresses. Keeping in view the importance of heat tolerance the current project was designed to inter-cross heat tolerant cotton genotypes to create sustainable tolerant genotypes through gene pyramiding. Heat tolerance is a quantitative trait which is governed by more genes, is difficult to inherit. A series of crosses is required to find a useful combination. The study particularly aimed to develop heat tolerant genotypes which could be used as a reliable heat tolerant material in future breeding programs.

Materials and methods

A set of seven genetic cotton populations were developed by schematic crossing (gene pyramiding) using heat and drought tolerant genotypes (Table 1). The genotypes were selfed to produce homozygous fixed genotypes. The developed root genotypes were evaluated under heat stress for two years. During the first year, all the genotypes were under normal and heat stressed environments and in the second year, same genotypes were subjected to normal and Heat + drought stressed conditions. To apply heat stress at the most critical stage of cotton i.e. flowering stage, a replicated set of genotypes were sown in the month of April to adjust flowering at high temperatures. The other set was sown in late June to surpass the period of high temperatures and heat waves. Drought stress was applied by reducing number of irrigations to 50% and halting irrigation water until symptoms of drought appeared on plants, followed by data recording related to drought stress. Morphological and physiological traits i.e., listed below were recorded from both treatments. The same set of genotypes was evaluated under normal and Heat + drought stress conditions in the next season. Similar traits, as mentioned above were recorded from three replications under normal and drought stress, respectively. All other recommended agronomic practices were same for both trials except for drought stress application. First, irrigation was applied on 3rd day of sowing. Second, third and fourth irrigation was applied at 9 days intervals. Further irrigation was followed at crop requirement. Recommended fertilizer dose 90 kg N, 35 g kg P2O5 and 38 kg K2O/acre was applied.

Table 1 Experimental material used in the study
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Morphological analysis

Following traits were reordered under normal as well as under stressed conditions during both years of evaluation. Plant Height (cm), Number of nodes, Internodal length (cm), Sympodial branches, Monopodial branches, Number of buds, Number of bolls, First fruiting branch, and Leaf area(cm2). Three newly born leaves from each plant were tagged and after 20 days, leaf area was measured using a portable Leaf Area Meter). Model: LAM-A. Average leaf area was then calculated.

Physiological analysis

The trait Relative Water Content was determined from each plant sample grown under normal as well as stressed conditions as by using [23].

$$\:RWC=100\:x\frac{\left(Fresh\:weight-dry\:weight\right)}{\left(\varvec{T}\varvec{u}\varvec{r}\varvec{g}\varvec{i}\varvec{d}\:\varvec{w}\varvec{e}\varvec{i}\varvec{g}\varvec{h}\varvec{t}-\varvec{D}\varvec{r}\varvec{y}\:\varvec{w}\varvec{e}\varvec{i}\varvec{g}\varvec{h}\varvec{t}\right)\:}$$

The trait Excised leaf water loss was calculated using the method provided by [24].

$$\:ELWL=\frac{Fresh\:Weight-Wilted\:Weight}{Dry\:Weight}$$

The trait Cell membrane stability of plant samples under normal as well as stressed conditions was assessed as by reciprocal of relative cell injury as by [25].

$$\:CMS\%=\left[\frac{\left\{1-\left(\frac{T1}{T2}\right)\right\}}{\left\{1-\left(\frac{C1}{C2}\right)\right\}}\right]x100$$

T1 = After-autoclaving stress sample conductance.

T2 = Stress sample conductance after to autoclaving.

C1 = Normal sample conductance prior to autoclaving.

C2 = Normal sample conductance after to autoclaving.

Molecular analysis

DNA extraction

DNA was extracted from all populations using CTAB method after 30 days of germination using standard method [26]. After extracting the plant DNA, DNA quantification was done using Nano-Drop ND-2000.

Polymerase chain reaction

All genotypes were screened using a set of 19heat/drought responsive transcription factors [27]. These included five heat shock proteins, one heat shock transcription factor, two dehydration responsive element binding proteins, one trehalose-6- phosphate synthase, NAC protein, MYB protein, WRKY protein, MMK protein, mitogen activated protein kinase, ascorbate peroxidase (APX) enzyme, annexin, and a phytochrome. Band scoring was done based on the presence or absence of transcription factors under study (Table 2).

Table 2 Mean values for Plant Height (PH), number of First Fruiting Branch(NFFB), Monopodial branches(MB), Sympodial branches(SB), Internodal Length(IL), number of bolls(NB), number of nodes(NN), Leaf Area(LA), relative water content(RWC), excise leaf water loss(ELWL), and cell membrane stability(CMS) under heat stress and normal conditions (in 2021)
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Statistical assessment

Analysis of variation (ANOVA) was recorded for all the traits under study as by [28]. Correlation was calculated for the all traits to check the association among the traits as used by [29]. The least significant difference (LSD) at P ≤ 0.05 was used to determine the significance of differences between the treatment means.

Results

Morphological assessment

In the first year, [(CIM-600×MNH-886)×MNH-1035)×IR-3701] showed maximum plant height i.e. 95.77 cm and 84.15 cm under normal as well as under stress conditions, respectively. First fruiting branch is very important trait while working against heat tolerance. The least first fruiting node was recorded in [(MNH-1035×MNH-886)×MNH-886)×SS-32] i.e. 7.60 in normal and 10.0 in stressed conditions. The genotype [(MNH-1035xMNH-886)×MNH-886)×SM-431] showed maximum number of bolls i.e. 27.75/plant under normal and 21.75/plant under heat stress conditions. Leaf area is another very important trait in heat stress scenarios. Leaf area is reduced when plants are in stress. [(CYTO-178×CIM-600)×MNH-1035)×FH-901], exhibited the smallest leaf area in heat stress i.e. 49.76 cm2 (Table 2). In the second year of evaluation, [(CYTO-178×CIM-600)×MNH-1035)] showed maximum plant height under both normal and drought/heat stress conditions i.e. 98.30 cm and 87.30 cm, respectively. [(CYTO-313×CIM-600)×CYTO-177)×NIAB-78] showed the maximum number of bolls under normal i.e. 35.67/plant, whereas, 17.00 number of bolls/plant were observed under drought/heat stress conditions (Table 3).

Table 3 Mean values for Plant Height (PH), number of First Fruiting Branch(NFFB), Monopodial branches(MB), Sympodial branches(SB), Internodal Length(IL), number of bolls(NB), number of nodes(NN), Leaf Area(LA), relative water content(RWC), excise leaf water loss(ELWL), and cell membrane stability(CMS) under heat stress and normal conditions (in 2022)
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Physiological assessment

Relative water content (RWC) is a very important physiological trait against heat and drought stress. In the first year of evaluation, the genotype [(CYTO-313×CIM-600)×CYTO-177)×NIAB-78] showed an improved RWC 72.31% under stressed conditions as compared to 66.92% under normal conditions. Similar genotype [(CYTO-313×CIM-600)×CYTO-177)×NIAB-78] showed the lowest Excise leaf water loss (ELWL) under normal and under stress in both years of evaluation. Cell Membrane Stability is the most important physiological parameter, which is often used as a screening tool for heat tolerance. The genotype [(CYTO-178×CIM-600)×MNH-1035)] showed improvement under stress 81.82% as compared to under normal conditions 74.81%. The genotype [(MNH-1035×MNH-886)×MNH-886)×SM-431] with the lowest CMS 47.27% also showed improvement in CMS 54.17% under stressed conditions (Table 2). In the second year of evaluation under drought/heat, an increasing trend was recorded for cell membrane stability for all the genotypes under drought stress as compared to normal conditions (Fig. 1). However, the genotype [(MNH-1035×MNH-886)×MNH-886)×SS-32] showed the highest CMS under both conditions (Fig. 1), (Table 3).

Fig. 1
figure 1

Average graphs for Physiological traits for all 7 genotypes for years 2021 (Normal & Heat Stress) and 2022 (Normal & Drought Stress)

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Molecular results

All seven developed genotypes parents were screened (Fig. 2), for 19 transcription factors related to heat and drought tolerance (GHSP26, HSP3, HSFA2, DREB1A, HSP101, DREB2A, GhNAC2, HSPCB, GhWRKY41, TPS, GbMYB5, ANNAT8, GhMPK17, GhMKK1, GhMKK3, GhMPK2, HSC70, APX1 and GhPP2A1). In parents, HSP101 was missing in VH-305, GHMK3 was absent in MNH-886, GhMYB3, GHMK3 and PK2 was absent in MNH-1035. The genotype FH-901 was also lacking GH MK3.PK 2 did not appeared in CIM-600 and DREBIA was not appear in IR-3701. Cyto-178 lacks GhMYB5, GHMKK3 and PK2. Whereas, the developed genotypes by crossing of these parents showed all the transcription factors under study (Table 4).

Table 4 Genotypes screening for 19 heat/drought transcription factors
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Fig. 2
figure 2

Screening of selected Genotypes with (a) HSP-101, (b) HSC-70 (c) ANNAT8

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Statistical analysis

All traits in both treatments were highly significant (Table 5). LSD was highly significant for both treatments for the traits of plant height, first fruiting branch, number of bolls, sympodial branches, relative water content, excised leaf water loss and cell membrane stability (Tables 2 and 3). Correlation analysis among traits depicted the association between plant height with intermodal length and sympodial branches. Internodal length was positively associated with number of nodes and sympodial branches and negatively associated with number of bolls in stress. Sympodial branches showed a strong positive association with number of nodes in stress. Number of bolls were positively associated with sympodial branches and with cell membrane stability (Table 6). A strong negative association was observed between number of bolls and the trait excised leaf water loss (Table 7).

Table 5 Analysis of Variance (ANOVA) for all the traits under study
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Table 6 Correlation analysis among Plant Height (PH), Number First Fruiting Branch(FFB), Internodal Length(IL, cm), number of nodes(NN), Monopodial branches(MB), Sympodial branches(SB), number of bolls(NB), Leaf Area(LA), relative water content(RWC, %), excise leaf water loss(ELWL) and cell membrane stability(CMS, %) under heat stress and normal conditions
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Table 7 Correlation analysis among Plant Height (PH), Internodal Length (IL, cm), Monopodial branches (MB), Sympodial branches (SB), number of nodes (NN), number of bolls (NB), relative water content (RWC, %), excise leaf water loss (ELWL) and cell membrane stability (CMS, %) under drought stress and normal conditions
Full size table

Discussion

In crop plants, heat stress alters the tertiary and quaternary structure of membrane proteins and increases membrane permeability [6], denaturation of proteins, synthesis of important macromolecules, photosynthesis, respiration, ion uptake, and mineral nutrition [30,31,32,33]. Heat stress tolerance is assessed through cell membrane stability in cotton [34, 35]. The improvement in cell membrane integrity against biotic and abiotic stimuli has been associated with heat shock proteins [36]. New genetic combinations were developed by crossing tolerant genotypes, following by making them homozygous. Theses genotypes depicted heat tolerance by showing an increasing trend in cell membrane integrity when exposed to heat stress as compared with normal conditions. Various morphological traits, including plant height, number of nodes, boll retention, and yield, express cotton growth under heat stress [37]. The squares and bolls retention are primarily decreased under heat and drought stresses [38, 39]. Water content regulates various physiological and metabolic processes in plants [40]; whereas, reduced water contents negatively affect plant growth [41]. Relative water content (RWC) is used as a measure of water content in the leaf tissue, as it shows plant’s ability to survive in water deficit conditions [42, 43]. A high RWC is preferred to keep water balance and used for selection to develop drought tolerant genotypes. ELWL shows cuticle thickness, as leaves lose water through the epidermis after being removed from the plant. A reduced rate of transpiration and less water loss from excised leaves are important for selection against drought stress [44]. Electrolyte leakage in plant leaves increases as a result of the drought stress [45]. Under drought stress, tolerant genotypes showed higher cell membrane stability index compared to susceptible genotypes [46]. CMT% can be used for screening and selection of cotton germplasm against heat stress [47]. Plants with higher cell membrane stability appeared with higher relative water content; predicting the traits being controlled by linked genes [48, 49] and lower excised leaf water loss values [49] shows RWC and ELWL as physiological indicators for CMS.

NFFB, an early-maturity trait is described as the number of nodes (cotyledon node excluded) with first fruiting branch [50]. It shows the relative photoperiodism and is linked to the flowering time [51]. NFFB is an effective morphological indicator for assessing cotton’s early maturity [52]. Improvement in cell membrane stability was also recorded under stress by some researchers [53,54,55,56]. But the sustainable solution is in the integration of conventional breeding and modern tools of plant breeding. Marker assisted gene pyramiding provided reliable genotypes which show improvement in heat tolerance probably because of combination of favorable alleles of the parent genotypes. The parent genotypes VH-305, MNH-886, CIM-600 [55], IR-370 showed drought tolerance [49], Cyto-178 depicted heat tolerant [57], FH-901 appeared drought susceptible [58]. However, the developed genetic combinations showed higher heat tolerance as compared to parental genotypes; it might be due to owing useful genetic accumulations. The transcription factors, related to heat and drought tolerance, missing in the parent genotypes, were appeared in new genetic combinations.

All the transcription factors under study were assembled in the genotypes through a series of systematic crossing. Stress-related transcription factors and genes regulate the plant physiological and biochemical processes to control crop growth and reproductive development. Among these transcription factors, GbMYB5 aids plant recovery from drought stress [59], GhMKK3 modulates stomatal responses [60], and GhWRKY41 boosts antioxidant production.

Conclusion

Cell membrane stability under heat stress may be used as a screening criterion for heat tolerance in cotton. The developed genotypes [(VH-305×MNH-886)×MNH-1035)×NIAB-78)], [(MNH-1035×MNH-886)×MNH-886)×SM-431] and [(MNH-1035×MNH-886)×MNH-886)×SS-32] shows heat tolerance under heat stress and may be used as heat tolerant material for cultivar development.

Data availability

Data will be provided on request by Muhammad Anwar and Muhammad Asif Saleem.

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Acknowledgements

The study was part of the NRPU research project of HEC entitled “Marker assisted gene pyramiding for heat tolerance in cotton” Project ID: 7965. We are thankful to Higher Education Commission Islamabad Pakistan for providing funds for this research work.

Funding

HEC Islamabad Pakistan (NRPU-7965), Hainan University Initiation Fund(XJ2400005264).

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Author notes

  1. Muhammad Anwar and Muhammad Asif Saleem equally contributed to this work.

Authors and Affiliations

  1. School of Tropical Agriculture and Forestry, School of Agriculture and Rural Affairs, School of Rural Revitalization), Hainan University, Haikou, China

    Muhammad Anwar

  2. Department of Plant Breeding and Genetics, B. Z. University Multan, Multan, Pakistan

    Muhammad Asif Saleem, Waqas Malik, Muhammad Qadir Ahmad, Mirza Muhammad Ahad Baig, Muhammad Asif & Muhammad Nauman

  3. Institute of Plant Breeding & Biotechnology (IPBB), Muhammad Nawaz Shareef University of Agriculture, Multan, 60000, Pakistan

    Sarmad Farogh Arshad

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  1. Muhammad Asif Saleem
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Contributions

Muhammad Asif Saleem conceived and designed the project. Muhammad Asif Saleem performed the experiments. Muhammad Anwar and Muhammad Saleem analyzed data. Muhammad Anwar, Muhammad Asif Saleem, Muhammad Asif, Muhammad Nauman, Mirza Muhammad Ahad Baig and Waqas Muhammad wrote the main manuscript. Sarmad Farogh Arshad, Mirza Muhammad Ahad Baig. Muhammad Asif Saleem and Muhammad Anwar supervised the study. Muhammad Anwar, Muhammad Asif Saleem, Muhamad Asif, Muhammad Numan, Mirza Muhammad Ahad Baig, Muhammad Qadir Ahmad and Muhammad waqas reviewed the manuscript.

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Correspondence to Muhammad Asif Saleem or Muhammad Anwar.

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Saleem, M.A., Malik, W., Ahmad, M.Q. et al. Gene pyramiding improved cell membrane stability under heat stress in cotton (Gossypium hirsutum L.). BMC Plant Biol 24, 886 (2024). https://doi.org/10.1186/s12870-024-05610-7

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BMC Plant Biology

ISSN: 1471-2229

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