Soybean plants enhance growth through metabolic regulation under heterogeneous drought stress

Heterogeneous drought stress (HED) is prevalent in drought-resistant practices such as deficit irrigation, root zone irrigation and strip intercropping. The mechanisms and improvement of crop drought resistance under HED are not fully understood. This study used double-root grafted Nandou 12 (ND12) soybean seedlings to simulate HED treatment under controlled conditions. Seedlings were transplanted into root cups with waterproof partitions to establish different soil moisture treatments: sufficient irrigation (SI) with 80 % soil moisture on both sides, HED with 80 % on one side and 40 % on the other, and homogeneous drought stress (HOD) with 60 % on both sides. The results indicated that soybean plants treated with HED exhibited healthier growth compared to those treated with HOD. Photosynthesis rate (Pn), stomatal conductance (cond.), transpiration rate (Tr), and relative water content (RWC) decreased by 10.24 %, 43.90 %, 152.66 %, and 8.69 % in HED-treated plants, respectively, but dry biomass increased by 3.38 %. Conversely, HOD conditions led to a significant decline in these parameters. Metabolomic and transcriptomic analyses revealed significant changes in the biosynthesis and signaling pathways of key phytohormones and metabolites, including abscisic acid (ABA), gibberellin (GA), jasmonic acid (JA), isoflavones, starch, and sugars. In HED-treated plants, GmNCED downregulation resulted in 54.22 % less ABA than HOD. GA levels increased under HED with upregulation of GmGA3OX1 and GmGA3OX2. JA content in HED-treated roots was 90.90 % higher than in HOD-treated roots. Isoflavones concentration including genistein (73.01 %), genistin (63.63 %), malonylgenistin (20.58 %), malonylgenistin (65 %), diadzin (38.15 %), and malonyldiadzin (47.61 %) levels, were significantly higher in HED-treated plants. Antioxidant enzyme activities indicated a 20 % increase in peroxidase (POD) activity under HED, while malondialdehyde (MDA) content was 27 % higher in HOD-treated plants, indicating greater oxidative stress. Chlorophyll content remained stable, and starch concentration increased by 33.33 % in HED-treated plants compared to HOD-treated plants. HED enhances phytohormonal responses and metabolic adjustments in soybean plants, boosting photosynthetic efficiency, antioxidant capabilities, growth, and drought resilience. This regulatory mechanism balances growth promotion and drought resistance, highlighting HED potential in improving crop resilience.